Physical developmental cues for the maturation of human pluripotent stem cell-derived cardiomyocytes

Stem Cell Research and Therapy

Volumn 5, Issue 1, 2014, Pages

  Zhu, Renjun ^a   Blazeski, Adriana ^a   Poon, Ellen ^b   Costa, Kevin D ^c   Tung, Leslie ^a   Boheler, Kenneth R ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; NERVE CELL ADHESION MOLECULE;

CALCIUM CURRENT; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL MATURATION; DESMOSOME; ELECTROSTIMULATION; EMBRYOID BODY; EXCITATION CONTRACTION COUPLING; EXTRACELLULAR MATRIX; GAP JUNCTION; HEART DEVELOPMENT; HEART HYPERTROPHY; HEART MITOCHONDRION; HEART RIGHT VENTRICLE DYSPLASIA; HUMAN; HUMAN EMBRYONIC STEM CELL; MECHANICAL STRESS; MECHANOTRANSDUCTION; MITOCHONDRIAL RESPIRATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW;

EID: 84988599499     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt507     Document Type: Review

References (139)

1. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
2. Okita K, Ichisaka T, Yamanaka S: Generation of germline-competent induced pluripotent stem cells. Nature 2007, 448:313-317.
3. Boheler KR: Pluripotency of human embryonic and induced pluripotent stem cells for cardiac and vascular regeneration. Thromb Haemost 2010, 104:23-29.
4. Lin S-L, Chang DC, Lin C-H, Ying S-Y, Leu D, Wu DTS: Regulation of somatic cell reprogramming through inducible mir-302 expression. Nucleic Acids Res 2011, 39:1054-1065.
5. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE: Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011, 8:376-388.
6. Burridge PW, Keller G, Gold JD, Wu JC: Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012, 10:16-28.
7. Mummery CL, Zhang J, Ng ES, Elliott DA, Elefanty AG, Kamp TJ: Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ Res 2012, 111:344-358.
8. Blazeski A, Zhu R, Hunter DW, Weinberg SH, Zambidis ET, Tung L: Cardiomyocytes derived from human induced pluripotent stem cells as models for normal and diseased cardiac electrophysiology and contractility. Prog Biophys Mol Biol 2012, 110:166-177.
9. Blazeski A, Zhu R, Hunter DW, Weinberg SH, Boheler KR, Zambidis ET, Tung L: Electrophysiological and contractile function of cardiomyocytes derived from human embryonic stem cells. Prog Biophys Mol Biol 2012,110:178-195.
10. Tulloch NL, Muskheli V, Razumova MV, Korte FS, Regnier M, Hauch KD, Pabon L, Reinecke H, Murry CE: Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 2011, 109:47-59.
11. Schaaf S, Shibamiya A, Mewe M, Eder A, Stöhr A, Hirt MN, Rau T, Zimmermann W-H, Conradi L, Eschenhagen T: Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One 2011, 6:e26397.
12. Zhang D, Shadrin IY, Lam J, Xian H-Q, Snodgrass HR, Bursac N: Tissueengineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 2013, 34:5813-5820.
13. Turnbull IC, Karakikes I, Serrao GW, Backeris P, Lee J-J, Xie C, Senyei G, Gordon RE, Li RA, Akar FG, Hajjar RJ, Hulot J-S, Costa KD: Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium. FASEB J 2014, 28:644-654.
14. Ebelt H, Jungblut M, Zhang Y, Kubin T, Kostin S, Technau A, Oustanina S, Niebrügge S, Lehmann J, Werdan K, Braun T: Cellular cardiomyoplasty: improvement of left ventricular function correlates with the release of cardioactive cytokines. Stem Cells 2007, 25:236-244.
15. Lieu DK, Fu J-D, Chiamvimonvat N, Tung KC, McNerney GP, Huser T, Keller G, Kong C-W, Li RA: Mechanism-based facilitated maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Arrhythm Electrophysiol 2013, 6:191-201.
16. Li S, Chen G, Li RA: Calcium signalling of human pluripotent stem cell-derived cardiomyocytes. J Physiol (Lond) 2013, 591:5279-5290.
17. Robertson C, Tran DD, George SC: Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells 2013, 31:829-837.
18. Yang X, Pabon L, Murry CE: Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 2014, 114:511-523.
19. Poon E, Yan B, Zhang S, Rushing S, Keung W, Ren L, Lieu DK, Geng L, Kong C-W, Wang J, Wong HS, Boheler KR, Li RA: Transcriptome-guided functional analyses reveal novel biological properties and regulatory hierarchy of human embryonic stem cell-derived ventricular cardiomyocytes crucial for maturation. PLoS One 2013, 8:e77784.
20. Wang N, Ingber DE: Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys J 1994, 66:2181-2189.
21. Ingber DE: Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 2003, 116:1157-1173.
22. Ingber DE: Tensegrity II: How structural networks influence cellular information processing networks. J Cell Sci 2003, 116:1397-1408.
23. Lele TP, Pendse J, Kumar S, Salanga M, Karavitis J, Ingber DE: Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J Cell Physiol 2006, 207:187-194.
24. Mammoto A, Ingber DE: Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol 2009, 21:864-870.
25. Kim D-H, Lipke EA, Kim P, Cheong R, Thompson S, Delannoy M, Suh K-Y, Tung L, Levchenko A: Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci U S A 2010, 107:565-570.
26. Street SF: Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 1983, 114:346-364.
27. Collinsworth AM, Zhang S, Kraus WE, Truskey GA: Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol Cell Physiol 2002, 283:C1219-C1227.
28. Kumar A, Chaudhry I, Reid MB, Boriek AM: Distinct signaling pathways are activated in response to mechanical stress applied axially and transversely to skeletal muscle fibers. J Biol Chem 2002, 277:46493-46503.
29. Simpson DG, Majeski M, Borg TK, Terracio L: Regulation of cardiac myocyte protein turnover and myofibrillar structure in vitro by specific directions of stretch. Circ Res 1999, 85:e59-e69.
30. Senyo SE, Koshman YE, Russell B: Stimulus interval, rate and direction differentially regulate phosphorylation for mechanotransduction in neonatal cardiac myocytes. FEBS Lett 2007, 581:4241-4247.
31. Taber LA: Biomechanics of cardiovascular development. Annu Rev Biomed Eng 2001, 3:1-25.
32. van den Berg G, Moorman AFM: Concepts of cardiac development in retrospect. Pediatr Cardiol 2009, 30:580-587.
33. Lopaschuk GD, Collins-Nakai RL, Itoi T: Developmental changes in energy substrate use by the heart. Cardiovasc Res 1992, 26:1172-1180.
34. Wiegerinck RF, Cojoc A, Zeidenweber CM, Ding G, Shen M, Joyner RW, Fernandez JD, Kanter KR, Kirshbom PM, Kogon BE, Wagner MB: Force frequency relationship of the human ventricle increases during early postnatal development. Pediatr Res 2009, 65:414-419.
35. Katz AM: Ernest Henry Starling, his predecessors, and the 'Law of the Heart'. Circulation 2002, 106:2986-2992.
36. Takahashi K, Kakimoto Y, Toda K, Naruse K: Mechanobiology in cardiac physiology and diseases. J Cell Mol Med 2013, 17:225-232.
37. Chicurel ME, Singer RH, Meyer CJ, Ingber DE: Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 1998, 392:730-733.
38. Shyy JY-J, Chien S: Role of integrins in endothelial mechanosensing of shear stress. Circ Res 2002, 91:769-775.
39. Samarel AM: Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 2005, 289:H2291-H2301.
40. Wozniak MA, Chen CS: Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009, 10:34-43.
41. Russell B, Curtis MW, Koshman YE, Samarel AM: Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J Mol Cell Cardiol 2010, 48:817-823.
42. Corda S, Samuel JL, Rappaport L: Extracellular matrix and growth factors during heart growth. Heart Fail Rev 2000, 5:119-130.
43. Sheikh F, Ross RS, Chen J: Cell-cell connection to cardiac disease. Trends Cardiovas Med 2009, 19:182-190.
44. LeGrice IJ, Takayama Y, Covell JW: Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. Circ Res 1995, 77:182-193.
45. Costa KD, Takayama Y, McCulloch AD, Covell JW: Laminar fiber architecture and three-dimensional systolic mechanics in canine ventricular myocardium. Am J Physiol Heart Circ Physiol 1999, 276:H595-H607.
46. Boycott HE, Barbier CSM, Eichel CA, Costa KD, Martins RP, Louault F, Dilanian G, Coulombe A, Hatem SN, Balse E: Shear stress triggers insertion of voltage-gated potassium channels from intracellular compartments in atrial myocytes. Proc Natl Acad Sci U S A 2013, 110:E3955-E3964.
47. Delmar M, McKenna WJ: The cardiac desmosome and arrhythmogenic cardiomyopathies: from gene to disease. Circ Res 2010, 107:700-714.
48. Saffitz JE: Arrhythmogenic cardiomyopathy: advances in diagnosis and disease pathogenesis. Circulation 2011, 124:e390-e392.
49. Gomes J, Finlay M, Ahmed AK, Ciaccio EJ, Asimaki A, Saffitz JE, Quarta G, Nobles M, Syrris P, Chaubey S, McKenna WJ, Tinker A, Lambiase PD: Electrophysiological abnormalities precede overt structural changes in arrhythmogenic right ventricular cardiomyopathy due to mutations in desmoplakin-A combined murine and human study. Eur Heart J 2012, 33:1942-1953.
50. Severs NJ, Bruce AF, Dupont E, Rothery S: Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 2008, 80:9-19.
51. Sheehy SP, Grosberg A, Parker KK: The contribution of cellular mechanotransduction to cardiomyocyte form and function. Biomech Model Mechanobiol 2012, 11:1227-1239.
52. Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan Y-N, Jan LY: Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 2007, 128:547-560.
53. Saffitz JE, Kléber AG: Effects of mechanical forces and mediators of hypertrophy on remodeling of gap junctions in the heart. Circ Res 2004, 94:585-591.
54. Peters N, Severs N, Rothery S, Lincoln C: Spatiotemporal relation between gap junctions and fascia adherens junctions during postnatal development of human ventricular myocardium. Circulation 1994, 90:713-725.
55. Vreeker A, van Stuijvenberg L, Hund TJ, Mohler PJ, Nikkels PGJ, van Veen TAB: Assembly of the cardiac intercalated disk during pre- and postnatal development of the human heart. PLoS One 2014, 9:e94722.
56. Guterl KA, Haggart CR, Janssen PM, Holmes JW: Isometric contraction induces rapid myocyte remodeling in cultured rat right ventricular papillary muscles. Am J Physiol Heart Circ Physiol 2007, 293:H3707-H3712.
57. Hove JR, Köster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M: Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 2003, 421:172-177.
58. Gherghiceanu M, Barad L, Novak A, Reiter I, Itskovitz-Eldor J, Binah O, Popescu LM: Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure. J Cell Mol Med 2011, 15:2539-2551.
59. Cao F, Wagner RA, Wilson KD, Xie X, Fu J-D, Drukker M, Lee A, Li RA, Gambhir SS, Weissman IL, Robbins RC, Wu JC: Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes. PLoS One 2008, 3:e3474.
60. Lundy SD, Zhu W-Z, Regnier M, Laflamme MA: Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev 2013, 22:1991-2002.
61. Sartiani L, Bettiol E, Stillitano F, Mugelli A, Cerbai E, Jaconi ME: Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 2007, 25:1136-1144.
62. Kamakura T, Makiyama T, Sasaki K, Yoshida Y, Wuriyanghai Y, Chen J, Hattori T, Ohno S, Kita T, Horie M, Yamanaka S, Kimura T: Ultrastructural maturation of human-induced pluripotent stem cell-derived cardiomyocytes in a long-term culture. Circ J 2013, 77:1307-1314.
63. Ou D-B, He Y, Chen R, Teng J-W, Wang H-T, Zeng D, Liu X-T, Ding L, Huang J-Y, Zheng Q-S: Three-dimensional co-culture facilitates the differentiation of embryonic stem cells into mature cardiomyocytes. J Cell Biochem 2011, 112:3555-3562.
64. Pal R, Mamidi MK, Das AK, Bhonde R: Comparative analysis of cardiomyocyte differentiation from human embryonic stem cells under 3-D and 2-D culture conditions. J Biosci Bioeng 2013, 115:200-206.
65. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A: Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 2007, 4:S60-S67.
66. Liau B, Christoforou N, Leong KW, Bursac N: Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function. Biomaterials 2011, 32:9180-9187.
67. Christoforou N, Liau B, Chakraborty S, Chellapan M, Bursac N, Leong KW: Induced pluripotent stem cell-derived cardiac progenitors differentiate to cardiomyocytes and form biosynthetic tissues. PLoS One 2013, 8:e65963.
68. Wong RCB, Pébay A, Nguyen LTV, Koh KLL, Pera MF: Presence of functional gap junctions in human embryonic stem cells. Stem Cells 2004, 22:883-889.
69. Wong RCB, Dottori M, Koh KLL, Nguyen LTV, Pera MF, Pébay A: Gap junctions modulate apoptosis and colony growth of human embryonic stem cells maintained in a serum-free system. Biochem Biophys Res Commun 2006, 344:181-188.
70. Kim JS, Kwon D, Hwang ST, Lee DR, Shim SH, Kim HC, Park H, Kim W, Han MK, Lee SH: hESC expansion and stemness are independent of connexin forty-three-mediated intercellular communication between hESCs and hASC feeder cells. PLoS One 2013, 8:e69175.
71. Moore JC, Tsang S-Y, Rushing SN, Lin D, Tse H-F, Chan CWY, Li RA: Functional consequences of overexpressing the gap junction Cx43 in the cardiogenic potential of pluripotent human embryonic stem cells. Biochem Biophys Res Commun 2008, 377:46-51.
72. Pekkanen-Mattila M, Chapman H, Kerkelä E, Suuronen R, Skottman H, Koivisto A-P, Aalto-Setälä K: Human embryonic stem cell-derived cardiomyocytes: demonstration of a portion of cardiac cells with fairly mature electrical phenotype. Exp Biol Med 2010, 235:522-530.
73. Zwi L, Caspi O, Arbel G, Huber I, Gepstein A, Park I-H, Gepstein L: Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation 2009, 120:1513-1523.
74. Caspi O, Itzhaki I, Kehat I, Gepstein A, Arbel G, Huber I, Satin J, Gepstein L: In vitro electrophysiological drug testing using human embryonic stem cell derived cardiomyocytes. Stem Cells Dev 2009, 18:161-172.
75. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L: Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004, 22:1282-1289.
76. Xue T, Cho HC, Akar FG, Tsang S-Y, Jones SP, Marbán E, Tomaselli GF, Li RA: 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 2005, 111:11-20.
77. Taha MF, Valojerdi MR, Hatami L, Javeri A: Electron microscopic study of mouse embryonic stem cell-derived cardiomyocytes. Cytotechnology 2012, 64:197-202.
78. Westfall MV, Pasyk KA, Yule DI, Samuelson LC, Metzger JM: Ultrastructure and cell-cell coupling of cardiac myocytes differentiating in embryonic stem cell cultures. Cell Motil Cytoskeleton 1997, 36:43-54.
79. Hakuno D, Takahashi T, Lammerding J, Lee RT: Focal adhesion kinase signaling regulates cardiogenesis of embryonic stem cells. J Biol Chem 2005, 280:39534-39544.
80. Karabekian Z, Gillum ND, Wong EWP, Sarvazyan N: Effects of N-cadherin overexpression on the adhesion properties of embryonic stem cells. Cell Adh Migr 2009, 3:305-310.
81. Saffitz JE: Dependence of electrical coupling on mechanical coupling in cardiac myocytes: insights gained from cardiomyopathies caused by defects in cell-cell connections. Ann N Y Acad Sci 2005, 1047:336-344.
82. Ishimine H, Yamakawa N, Sasao M, Tadokoro M, Kami D, Komazaki S, Tokuhara M, Takada H, Ito Y, Kuno S, Yoshimura K, Umezawa A, Ohgushi H, Asashima M, Kurisaki A: N-Cadherin is a prospective cell surface marker of human mesenchymal stem cells that have high ability for cardiomyocyte differentiation. Biochem Biophys Res Commun 2013, 438:753-759.
83. Kim C, Wong J, Wen J, Wang S, Wang C, Spiering S, Kan NG, Forcales S, Puri PL, Leone TC, Marine JE, Calkins H, Kelly DP, Judge DP, Chen H-SV: Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs. Nature 2013, 494:105-110.
84. Decker ML, Janes DM, Barclay MM, Harger L, Decker RS: Regulation of adult cardiocyte growth: effects of active and passive mechanical loading. Am J Physiol 1997, 272:H2902-H2918.
85. Sadoshima J, Izumo S: The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol 1997, 59:551-571.
86. Yamamoto K, Dang QN, Maeda Y, Huang H, Kelly RA, Lee RT: Regulation of cardiomyocyte mechanotransduction by the cardiac cycle. Circulation 2001, 103:1459-1464.
87. Balakumar P, Jagadeesh G: Multifarious molecular signaling cascades of cardiac hypertrophy: can the muddy waters be cleared? Pharmacol Res 2010, 62:365-383.
88. Jacot JG, McCulloch AD, Omens JH: Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 2008, 95:3479-3487.
89. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang H-Y, Speicher DW, Sanger JW, Sanger JM, Discher DE: Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 2008, 121:3794-3802.
90. Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T: Tissue engineering of a differentiated cardiac muscle construct. Circ Res 2002, 90:223-230.
91. Costa KD, Holmes JW, McCulloch AD: Modelling cardiac mechanical properties in three dimensions. Phil Trans R Soc A 2001, 359:1233-1250.
92. Salick MR, Napiwocki BN, Sha J, Knight GT, Chindhy SA, Kamp TJ, Ashton RS, Crone WC: Micropattern width dependent sarcomere development in human ESC-derived cardiomyocytes. Biomaterials 2014, 35:4454-4464.
93. Baudino TA, Carver W, Giles W, Borg TK: Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol 2006, 291:H1015-H1026.
94. Radisic M, Park H, Martens TP, Salazar-Lazaro JE, Geng W, Wang Y, Langer R, Freed LE, Vunjak-Novakovic G: Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res 2008, 86:713-724.
95. Vliegen HW, van der Laarse A, Cornelisse CJ, Eulderink F: Myocardial changes in pressure overload-induced left ventricular hypertrophy. A study on tissue composition, polyploidization and multinucleation. Eur Heart J 1991, 12:488-494.
96. Kadota S, Minami I, Morone N, Heuser JE, Agladze K, Nakatsuji N: Development of a reentrant arrhythmia model in human pluripotent stem cell-derived cardiac cell sheets. Eur Heart J 2013, 34:1147-1156.
97. Hazeltine LB, Badur MG, Lian X, Das A, Han W, Palecek SP: Temporal impact of substrate mechanics on differentiation of human embryonic stem cells to cardiomyocytes. Acta Biomater 2014, 10:604-612.
98. Gwak S-J, Bhang SH, Kim I-K, Kim S-S, Cho S-W, Jeon O, Yoo KJ, Putnam AJ, Kim B-S: The effect of cyclic strain on embryonic stem cell-derived cardiomyocytes. Biomaterials 2008, 29:844-856.
99. Kensah G, Roa Lara A, Dahlmann J, Zweigerdt R, Schwanke K, Hegermann J, Skvorc D, Gawol A, Azizian A, Wagner S, Maier LS, Krause A, Dräger G, Ochs M, Haverich A, Gruh I, Martin U: Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur Heart J 2013, 34:1134-1146.
100. Mihic A, Li J, Miyagi Y, Gagliardi M, Li S-H, Zu J, Weisel RD, Keller G, Li R-K: The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 2014, 35:2798-2808.
101. Thavandiran N, Dubois N, Mikryukov A, Masse S, Beca B, Simmons CA, Deshpande VS, McGarry JP, Chen CS, Nanthakumar K, Keller GM, Radisic M, Zandstra PW: Design and formulation of functional pluripotent stem cellderived cardiac microtissues. Proc Natl Acad Sci U S A 2013, 110:E4698-E4707.
102. Chan Y-C, Ting S, Lee Y-K, Ng K-M, Zhang J, Chen Z, Siu C-W, Oh SKW, Tse H-F: Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells. J Cardiovasc Trans Res 2013, 6:989-999.
103. Hirt MN, Boeddinghaus J, Mitchell A, Schaaf S, Börnchen C, Müller C, Schulz H, Hubner N, Stenzig J, Stoehr A, Neuber C, Eder A, Luther PK, Hansen A, Eschenhagen T: Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J Mol Cell Cardiol 2014, 74C:151-161.
104. Chen MQ, Xie X, Wilson KD, Sun N, Wu JC, Giovangrandi L, Kovacs GTA: Current-controlled electrical point-source stimulation of embryonic stem cells. Cell Mol Bioeng 2009, 2:625-635.
105. Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G: Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 2004, 101:18129-18134.
106. Sathaye A, Bursac N, Sheehy S, Tung L: Electrical pacing counteracts intrinsic shortening of action potential duration of neonatal rat ventricular cells in culture. J Mol Cell Cardiol 2006, 41:633-641.
107. Chiu LLY, Iyer RK, King J-P, Radisic M: Biphasic electrical field stimulation aids in tissue engineering of multicell-type cardiac organoids. Tissue Eng A 2011, 17:1465-1477.
108. Lasher RA, Pahnke AQ, Johnson JM, Sachse FB, Hitchcock RW: Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype. J Tissue Eng 2012, 3:2041731412455354.
109. Johnson TB, Kent RL, Bubolz BA, McDermott PJ: Electrical stimulation of contractile activity accelerates growth of cultured neonatal cardiocytes. Circ Res 1994, 74:448-459.
110. Bers DM: Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 2008, 70:23-49.
111. Serena E, Figallo E, Tandon N, Cannizzaro C, Gerecht S, Elvassore N, Vunjak-Novakovic G: Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Exp Cell Res 2009, 315:3611-3619.
112. Sauer H, Rahimi G, Hescheler J, Wartenberg M: Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem 1999, 75:710-723.
113. Martherus RSRM, Vanherle SJV, Timmer EDJ, Zeijlemaker VA, Broers JL, Smeets HJ, Geraedts JP, Ayoubi TAY: Electrical signals affect the cardiomyocyte transcriptome independently of contraction. Physiol Genomics 2010, 42A:283-289.
114. Yang J, Holman GD: Insulin and contraction stimulate exocytosis, but increased AMP-activated protein kinase activity resulting from oxidative metabolism stress slows endocytosis of GLUT4 in cardiomyocytes. J Biol Chem 2005, 280:4070-4078.
115. Xia Y, Buja LM, Scarpulla RC, McMillin JB: Electrical stimulation of neonatal cardiomyocytes results in the sequential activation of nuclear genes governing mitochondrial proliferation and differentiation. Proc Natl Acad Sci U S A 1997, 94:11399-11404.
116. Foldes G, Mioulane M, Wright JS, Liu AQ, Novak P, Merkely B, Gorelik J, Schneider MD, Ali NN, Harding SE: Modulation of human embryonic stem cell-derived cardiomyocyte growth: a testbed for studying human cardiac hypertrophy? J Mol Cell Cardiol 2011, 50:367-376.
117. Heineke J, Molkentin JD: Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006, 7:589-600.
118. Morgan KY, Black LD: Mimicking isovolumic contraction with combined electromechanical stimulation improves the development of engineered cardiac constructs. Tissue Eng A 2014, 20:1654-1667.
119. Park H, Larson BL, Kolewe ME, Vunjak-Novakovic G, Freed LE: Biomimetic scaffold combined with electrical stimulation and growth factor promotes tissue engineered cardiac development. Exp Cell Res 2014, 321:297-306.
120. Rana P, Anson B, Engle S, Will Y: Characterization of human-induced pluripotent stem cell-derived cardiomyocytes: bioenergetics and utilization in safety screening. Toxicol Sci 2012, 130:117-131.
121. 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: Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013, 12:127-137.
122. Folmes CDL, Nelson TJ, Dzeja PP, Terzic A: Energy metabolism plasticity enables stemness programs. Ann N Y Acad Sci 2012, 1254:82-89.
123. Facucho-Oliveira JM, St John JC: The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 2009, 5:140-158.
124. Folmes CDL, Dzeja PP, Nelson TJ, Terzic A: Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 2012, 11:596-606.
125. Cho YM, Kwon S, Pak YK, Seol HW, Choi YM, Park DJ, Park KS, Lee HK: Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 2006, 348:1472-1478.
126. Prowse ABJ, Chong F, Elliott DA, Elefanty AG, Stanley EG, Gray PP, Munro TP, Osborne GW: Analysis of mitochondrial function and localisation during human embryonic stem cell differentiation in vitro. PLoS One 2012, 7:e52214.
127. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U: Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 2011, 29:486-495.
128. Lopaschuk GD, Jaswal JS: Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J Cardiovasc Pharmacol 2010, 56:130-140.
129. Porter GA Jr, Hom JR, Hoffman DL, Quintanilla RA, de M Bentley KL, Sheu S-S: Bioenergetics, mitochondria, and cardiac myocyte differentiation. Prog Pediatr Cardiol 2011, 31:75-81.
130. Kim C, Majdi M, Xia P, Wei KA, Talantova M, Spiering S, Nelson B, Mercola M, Chen H-SV: Non-cardiomyocytes influence the electrophysiological maturation of human embryonic stem cell-derived cardiomyocytes during differentiation. Stem Cells Dev 2010, 19:783-795.
131. Müller F-J, Schuldt BM, Williams R, Mason D, Altun G, Papapetrou EP, Danner S, Goldmann JE, Herbst A, Schmidt NO, Aldenhoff JB, Laurent LC, Loring JF: A bioinformatic assay for pluripotency in human cells. Nat Methods 2011, 8:315-317.
132. Lahti AL, Kujala VJ, Chapman H, Koivisto AP, Pekkanen-Mattila M, Kerkela E, Hyttinen J, Kontula K, Swan H, Conklin BR, Yamanaka S, Silvennoinen O, Aalto-Setala K: Model for long QT syndrome type 2 using human iPS cells demonstrates arrhythmogenic characteristics in cell culture. Dis Model Mech 2012, 5:220-230.
133. Matsa E, Dixon JE, Medway C, Georgiou O, Patel MJ, Morgan K, Kemp PJ, Staniforth A, Mellor I, Denning C: Allele-specific RNA interference rescues the long-QT syndrome phenotype in human-induced pluripotency stem cell cardiomyocytes. Eur Heart J 2014, 35:1078-1087.
134. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LIR, Yabuuchi A, Takeuchi A, Cunniff KC, Hongguang H, McKinney-Freeman S, Naveiras O, Yoon TJ, Irizarry RA, Jung N, Seita J, Hanna J, Murakami P, Jaenisch R, Weissleder R, Orkin SH, Weissman IL, Feinberg AP, Daley GQ: Epigenetic memory in induced pluripotent stem cells. Nature 2010, 467:285-290.
135. Kim K, Zhao R, Doi A, Ng K, Unternaehrer J, Cahan P, Huo H, Loh Y-H, Aryee MJ, Lensch MW, Li H, Collins JJ, Feinberg AP, Daley GQ: Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat Biotechnol 2011, 29:1117-1119.
136. Levin M, Stevenson CG: Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu Rev Biomed Eng 2012, 14:295-323.
137. Uosaki H, Fukushima H, Takeuchi A, Matsuoka S, Nakatsuji N, Yamanaka S, Yamashita JK: Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 2011, 6:e23657.
138. Dubois NC, Craft AM, Sharma P, Elliott DA, Stanley EG, Elefanty AG, Gramolini A, Keller G: SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol 2011, 29:1011-1018.
139. Boheler KR, Bhattacharya S, Kropp EM, Chuppa S, Riordon DR, Bausch-Fluck D, Burridge PW, Wu JC, Wersto RP, Chan GCF, Rao S, Wollscheid B, Gundry RL: A human pluripotent stem cell surface N-glycoproteome resource reveals new markers, extracellular epitopes, and drug targets. Stem Cell Reports 2014, 3:185-203.