Human embryonic stem cell-derived cardiomyocytes: Drug discovery and safety pharmacology

Expert Opinion on Drug Discovery

Volumn 2, Issue 5, 2007, Pages 739-753

  He, Jia Qiang ^a   January, Craig T ^a,b   Thomson, James A ^a,c,d,e   Kamp, Timothy J ^a,b,e  

^a Cellular Dynamics International Inc   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN   (United States)

^e WiCell Research Institute   (United States)

Author keywords

Action potential; Adult stem cell; Cardiomyocytes; Directed differentiation; Drug discovery; Electrophysiology; Embryoid body; Genetic manipulation; hERG; Human embryonic stem cell; In vitro cellular assays; QT prolongation

Indexed keywords

AMIODARONE; SMALL INTERFERING RNA; VERAPAMIL;

ACTION POTENTIAL; CALCIUM TRANSPORT; CARDIOTOXICITY; CELL ASSAY; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL SELECTION; CELL TYPE; DISEASE ASSOCIATION; DISEASE MODEL; DRUG SAFETY; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; GENETIC ENGINEERING; HEART MUSCLE CELL; HEART PROARRHYTHMIA; HIGH THROUGHPUT SCREENING; HUMAN; IN VITRO STUDY; LONG QT SYNDROME; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN TARGETING; QT PROLONGATION; REVIEW; RISK ASSESSMENT;

EID: 34447571881     PISSN: 17460441     EISSN: None     Source Type: Journal    
DOI: 10.1517/17460441.2.5.739     Document Type: Review

References (91)

1. EVANS MJ, KAUFMAN MH: Establishment in culture of pluripotential cells from mouse embryos. Nature (1981) 292(5819):154-156.
2. MARTIN GR: Isolation of a pluripotent cell fine from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA (1981) 78(12):7634-7638.
3. THOMSON JA, ITSKOVITZ-ELDOR J, SHAPIRO SS et al.: Embryonic stem cell lines derived from human blastocysts. Science (1998) 282(5391):1145-1147.
4. MARSHALL VS, WAKNITZ MA, THOMSON JA: Isolation and maintenance of primate embryonic stem cells. Methods Mol. Biol. (2001) 158:11-18.
5. WILLIAMS RL, HILTON DJ, PEASE S et al.: Myeloid leukemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature(1988) 336(6200):684-687.
6. AMIT M, SHARIKI C, MARGULETS V, ITSKOVITZ-ELDOR J: Feeder layer- and serum-free culture of human embryonic stem cells. Biol. Reprod. (2004) 70(3):837-845.
7. XU RH, PECK RM, LI DS et al.: Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat. Methods (2005) 2(3):185-190.
8. XU C, ROSLER E, JIANG J et al.: Basic fibroblast growth factor supports undifferentiated human embryonic stem cell growth without conditioned medium. Stem Cells (2005) 23(3):315-323.
9. WANG L, LI L, MENENDEZ P, CERDAN C, BHATIA M: Human embryonic stem cells maintained in the absence of mouse embryonic fibfoblasts or conditioned media are capable of hematopoietic development. Blood (2005) 105(12):4598-4603.
10. BEATTIE GM, LOPEZ AD, BUCAY N et al.: Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells(2005) 23(4):489-495.
11. VALLIER L, ALEXANDER M, PEDERSEN RA: Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci. (2005) 118(Pt 19):4495-4509.
12. LUDWIG TE, BERGENDAHL V, LEVENSTEIN ME et al.: Feeder-independent culture of human embryonic stem cells. Nat. Methods (2006) 3(8):637-646.
13. 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. USA (2006) 103(18):6907-6912.
14. LU J, HOU R, BOOTH CJ, YANG SH, SNYDER M: Defined culture conditions of human embryonic stem cells. Proc. Natl. Acad, Sci. USA (2006) 103(15):5688-5693.
15. FORTIER LA: Stem cells: classifications, controversies, and clinical applications. Vet. Surg. (2005) 34(5):415-423.
16. FRASER JK, SCHREIBER RE, ZUK PA, HEDRICK MH: Adult stem cell therapy for the heart. Int. J. Biachem. Cell Biol. (2004) 36(4):658-666.
17. PASSIER R, MUMMERY C: Cardiomyocyte differentiation from embryonic and adult stem cells. Curr. Opin. Biotechnol. (2005) 16(5):498-502.
18. BRIMBLE SN, ZENG X, WEILER DA et al.: Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev. (2004) 13(6):585-597.
19. DRAPER JS, SMITH K, GOKHALE P et al.: Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. (2004) 22(1):53-54.
20. ZWAKA TP, THOMSON JA: Homologous recombination in human embryonic stem cells. Nat. Biotechnol. (2003) 21(3):319-321.
21. MALTSEV VA, ROHWEDEL J, HESCHELER J, WOBUS AM: Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech. Dev. (1993) 44(1):41-50.
22. 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. (2001) 108(3):407-414.
23. HE JQ, MA Y, LEE Y, THOMSON JA, KAMP TJ: Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Cirr. Res. (2003) 93(1):32-39.
24. 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. Circulation (2003) 107(21):2733-2740.
25. XU C, POLICE S, RAO N, CARPENTER MK: Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res. (2002) 91(6):501-508.
26. HENG BC, HAIDER HK. SIM EK, CAO T, NG SC: Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc. Res. (2004) 62(1):34-42.
27. EISENBERG CA, MARKWALD RR: Mixed cultures of avian blastoderm cells and the quail mesoderm cell line QCE-6 provide evidence for the pluripotentiality of early mesoderm. Dev. Biol. (1997) 191(2):167-181.
28. VAN DEN EIJNDEN-VAN RAAIJ AJ, VAN ACHTERBERG TA, VAN DER KRUIJSSEN CM et al.: Differentiation of aggregated murine P19 embryonal carcinoma cells is induced by a novel visceral endoderm-specific FGF-like factor and inhibited by activin A. Mech. Dev. (1991) 33(2):157-165.
29. PASSIER R, OOSTWAARD DW, SNAPPER J et al.: Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells (2005) 23(6):772-780.
30. YAMASHITA JK, TAKANO M, HIRAOKA-KANIE M et al.: Prospective identification of cardiac progenitors by a novel single cell-based cardiomyocyte induction. FASEB J (2005) 19(11):1534-1536.
31. BOHELER KR, CZYZ J, TWEEDIE D et al.: Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ. Res. (2002) 91(3):189-201.
32. WOBUS AM, ROHWEDEL J, MALTSEV V, HESCHELER J: Development of cardiomyocytes expressing cardiac-specific genes, action potentials, and ionic channels during embryonic stem cell-derived cardiogenesis. Ann. N Y Acad. Sci. (1995) 752:460-469.
33. ZEINEDDINE D, PAPADIMOU E, CHEBLI K et al.: Oct-3/4 dose dependently regulates specification of embryonic stem cells toward a cardiac lineage and early heart development. Dev. Cell (2006) 11(4):535-546.
34. YUASA S, ITABASHI Y, KOSHIMIZU U et al.: Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. (2005) 23(5):607-611.
35. MCDEVITT TC, LAFLAMME MA, MURRY CE: Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway. J. Mol. Cell Cardiol. (2005) 39(6):865-873.
36. SACHINIDIS A, GISSEL C, NIERHOFF D et al.: Identification of platelet-derived growth factor-BB as cardiogenesis-inducing factor in mouse embryonic stem cells under serum-free conditions. Cell Physiol. Biochem. (2003) 13(6):423-429.
37. DELL'ERA P. RONCA R, COCO L et al.: Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circ. Res. (2003) 93(5):414-420.
38. WU H, LEE SH, GAO J, LIU X, IRUELA-ARISPE ML: Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development (1999) 126(16):3597-3605.
39. SACHINIDIS A, KOLOSSOV E, FLEISCHMANN BK, HESCHELER J: Generation of cardiomyocytes from embryonic stem cells experimental studies. Herz (2002) 27(7):589-597.
40. PARISI S, D'ANDREA D, LAGO CT et al.: Nodal-dependent Cripto signaling promotes cardiomyogenesis and redirects the neural Fate of embryonic stem cells. J Cell Biol. (2003) 163(2):303-314.
41. PAQUIN J, DANALACHE BA, JANKOWSKI M, MCCANN SM, GUTKOWSKA J: Oxytocin induces differentiation of P19 embryonic stem cells to cardiomyocytes. Proc. Natl. Acad. Sci. USA (2002) 99(14):9550-9555.
42. VENTURA C, ZINELLU E, MANINCHEDDA E, MAIOLI M: Dynorphin B is an agonist of nuclear opioid receptors coupling nuclear protein kinase C activation to the transcription of cardiogenic genes in GTR1 embryonic stem cells. Circ. Res. (2003) 92(6):623-629.
43. RODRIGUEZ ER, TAN CD, ONWUTA US, PARRILLO JE: Cardiac myocyte differentiation induced by 3,5,3′-triiodo-L-thyronine (T3) in P19 teratocarcinoma cells is accompanied by preferential binding of RGG(T/ A)CA direct repeats spaced by 4 base pairs in the DNA. Biochem. Biophys. Res. Commun. (1994) 205(3):1899-1906.
44. SAUER H, NEUKIRCHEN W, RAHIMI G et al.: Involvement of reactive oxygen species in cardiotrophin-1-induced proliferation of cardiomyocytes differentiated from murine embryonic stem cells. Exp. Cell Res. (2004) 294(2):313-324.
45. BURRIDGE PW, ANDERSON D, PRIDDLE H et al.: Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights inter-line variability. Stem Cells (2006).
46. CHOI SC, YOON J, SHIM WJ, RO YM, LIM DS: 5-azacytidine induces cardiac differentiation of P19 embryonic stem cells. Exp. Mol. Med. (2004) 36(6):515-523.
47. TAKAHASHI T, LORD B, SCHULZE PC et al.: Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation (2003) 107(14):1912-1916.
48. WOBUS AM, KAOMEI G, SHAN J et al.: Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol, Cell Cardiol. (1997) 29(6):1525-1539.
49. ZANDSTRA PW, BAUWENS C, YIN T et al.: Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng. (2003) 9(4):767-778.
50. SKERJANC IS, PETROPOULOS H, RIDGEWAY AG, WILTON S: Myocyte enhancer factor 2C and Nkx2-5 up-regulace each other's expression and initiate cardiomyogenesis in P19 cells. J. Biol. Chem. (1998) 273(52):34904-34910.
51. YOON BS, YOO SJ, LEE JE et al.: Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation (2006) 74(4):149-159.
52. KADIVAR M, KHATAMI S, MORTAZAVI Y et al.: In vitro cardiomyogenic potential of human umbilical vein-derived mesenchymal stem cells. Biochem. Biophys. Res. Commun. (2006) 340(2):639-647.
53. OH H, BRADFUTE SB, GALLARDO TD et al.: Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad Sci. USA (2003) 100(21):12313-12318.
54. + progenitor cells highly purified by magnetic-activated cell sorting. Bone Marrow Transplant. (1998) 21(10):987-993.
55. KLUG MG, SOONPAA MH, KOH GY, FIELD LJ: Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin. Invest. (1996) 98(1):216-224.
56. ZWEIGERDT R. BURG M, WILLBOLD E, ABTS H, RUEDIGER M: Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy (2003) 5(5):399-413.
57. METZGER JM, LIN WI, SAMUELSON LC: Vital staining of cardiac myocytes during embryonic stem cell cardiogenesis in vitro. Circ. Res. (1996) 78(4):547-552.
58. HIDAKA K, LEE JK, KIM HS et al.: Chamber-spccific differentiation of Nkx2.5-positive cardiac precursor cells from murine embryonic stem cells. FASEB J. (2003) 17(6):740-742.
59. KOLOSSOV E, FLEISCHMANN BK, LIU Q et al.: Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue-specific expression of the green fluorescent protein. J. Cell Biol. (1998) 143(7):2045-2056.
60. KOLOSSOV E, LU Z, DROBINSKAYA I et al.: Identification and characterization of embryonic stem cell-derived pacemaker and atrial cardiomyocytes. FASEB J. (2005) 19(6):577-579.
61. MULLER M, FLEISCHMANN BK, SELBERT S et al.: Selection of ventricular-like cardiomyocytes from ES cells in vitro. FASEB J. (2000) 14(15):2540-2548.
62. MEYER N, JACONI M, LANDOPOULOU A, FORT P, PUCEAT M: A fluorescent reporter gene as a marker for ventricular specification in ES-derived cardiac cells. FEBS Lett. (2000) 478(1-2):151-158.
63. SCHROEDER M, NIEBRUEGGE S, WERNER A et al.: Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol, Bioeng. (2005) 92(7):920-933.
64. 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. (2006) 15(5):631-639.
65. GIMOND C, MARCHETTI S, PAGES G: Differentiation of mouse embryonic stem cells into endothelial cells: genetic selection and potential use in vivo. Methods Mol. Biol. (2006) 330:303-329.
66. CASPI O, GEPSTEIN L: Potential applications of human embryonic stem ccll-derived cardiomyocytes. Ann. N Y Acad. Sci. (2004) 1015:285-298.
67. NATTEL S: Atrial elcctrophysiologic remodeling caused by rapid atrial activation: underlying mechanisms and clinical relevance to atrial fibrillation. Cardiovasc. Res. (1999) 42(2):298-308.
68. SCHRAM G, POURRIER M, MELNYK P, NATTEL S: Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ. Res. (2002) 90(9):939-950.
69. KEHAT I, GEPSTEIN A. SPIRA A. ITSKOVITZ-ELDOR J, GEPSTEIN L: High-resolution electrophysiologic assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ. Res. (2002) 91(8):659-661.
70. SATIN J, KEHAT I, CASPI O et al.: Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. J Physiol. (2004) 559(Pt 2):479-496.
71. 2+ handling and the role of sarcoplasmic reticulum in the contraction. Stem Cells (2006) 24(2):236-245.
72. MINAMINO T. YUJIRI T, PAPST PJ et al.: MEKK1 suppresses oxidative stress-induced apoptosis of embryonic stem cell-derived cardiac myocytes. Proc. Natl. Acad. Sci. USA (1999) 96(26):15127-15132.
73. LORICO A. RAPPA G, FLAVELL RA, SARTORELLI AC: Double knockout of the MRP gene leads to increased drug sensitivity in vitro. Cancer Res. (1996) 56(23):5351-5355.
74. DE VRIES A. FLORES ER. MIRANDA B et al.: Targeted point mutations of p53 lead to dominant-negative inhibition of wild-type p53 function. Proc. Natl. Acad. Sci. USA (2002) 99(5):2948-2953.
75. DELISLE BP, ANSON BD, RAJAMANI S, JANUARY CT: Biology of cardiac arrhythmias: ion channel protein trafficking. Circ. Res (2004) 94(11):1418-1428.
76. MORGANROTH J, BROWN AM, CRITZ S et al.: Variability of the QTc interval: impact on defining drug effect and low-frequency cardiac event. Am J. Cardiol. (1993) 72(6):26B-31B.
77. CUBEDDU LX: QT prolongation and fatal arrhythmias: a review of clinical implications and effects of drugs. Am. J. Ther. (2003) 10(6):452-457.
78. WYSOWSKI DK, SWARTZ L: Adverse drug event surveillance and drug withdrawals in the United States, 1969-2002: the importance of reporting suspected reactions. Arch. Intern. Med. (2005) 165(12):1363-1369.
79. JANUARY CT, FOZZARD HA. Delayed after depolarizations in heart muscle: mechanisms and relevance. Pharmarol, Rev. (1988) 40(3):219-227.
80. 2+ current. Cirr. Res. (1989) 64(5):977-990.
81. JANUARY CT, CHAU V, MAKIELSKI JC: Triggered activity in the heart: cellular mechanisms of early after-depolarizations. Eur. Heart J. (1991) 12(Suppl. F):4-9.
82. JANUARY CT, MOSCUCCI A: Cellular mechanisms of early after depolarizations. Ann. N Y Acad. Sci. (1992) 644:23-32.
83. STUDENIK CR, ZHOU Z, JANUARY CT: Differences in action potential and early after depolarization properties in LQT2 and LQT3 models of long QT syndrome. Br. J. Pharmacol. (2001) 132(1):85-92.
84. EBINGER MW, KRISHNAN S, SCHUGER CD: Mechanisms of ventricular arrhythmias in heart failure. Curr. Heart Fail. Rep. (2005) 2(3):111-117.
85. JOSHI A, DIMINO T, VOHRA Y, CUI C, YAN GX: Predinical strategies to assess QT liability and torsadogenic potential of new drugs: the role of experimental models. J. Electrocardiol. (2004) 37(Suppl.):7-14.
86. YANG T, SNYDERS D, RODEN DM: Drug block of I(kr): model systems and relevance to human arrhythmias. J. Cardiovasc. Pharmacol. (2001) 38(5):737-744.
87. HONDEGHEM LM, CARLSSON L, DUKER G: Instability and triangulation of the action potential predict serious proarrhythmia, but action potential duration prolongation is antiarrhythmic. Circulation (2001) 103(15):2004-2013.
88. DE PONTI F, POLUZZI E, CAVALLI A, RECANATINI M, MONTANARO N: Safety of non-antiarrhythmic drugs that prolong the QT interval or induce torsade de pointes: an overview. Drug Saf. (2002) 25(4):263-286.
89. NORSTROM A, AKESSON K, HARDARSON T et al.: Molecular and pharmacological properties of human embryonic stem cell-derived cardiomyocytes. Exp. Biol. Med. (Maywood) (2006) 231(11):1753-1762.
90. BAHARVAND H, AZARNIA M, PARIVAR K, ASHTIANI SK: The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. J. Mol. Cell Cardiol. (2005) 38(3):495-503.
91. ZIMMERMANN WH, SCHNEIDERBANGER K, SCHUBERT P et al.: Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. (2002) 90(2):223-230.