Biomaterial based cardiac tissue engineering and its applications

Biomedical Materials (Bristol)

Volumn 10, Issue 3, 2015, Pages

  Huyer, Locke Davenport ^a,b   Montgomery, Miles ^a,b   Zhao, Yimu ^a,b   Xiao, Yun ^a,b   Conant, Genevieve ^a,b   Korolj, Anastasia ^a   Radisic, Milica ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

biomaterials; cardiac tissue engineering; host response; in vitro drug screening

Indexed keywords

BIOMATERIALS; CARDIOLOGY; CELL DEATH; CELL ENGINEERING; COMPLEX NETWORKS; DIAGNOSIS; DISEASES; HEART; OXYGEN SUPPLY; PROFESSIONAL ASPECTS; TISSUE; TISSUE ENGINEERING;

BIOMATERIAL SCAFFOLDS; CARDIAC TISSUE ENGINEERING; CARDIO-VASCULAR DISEASE; COMPLEX RELATIONSHIPS; DRUG SCREENING; HOST RESPONSE; MYOCARDIAL INFARCTION; REGENERATIVE MEDICINE;

SCAFFOLDS (BIOLOGY);

ALGINIC ACID; BIOMATERIAL; CALCIUM CHANNEL L TYPE; CARBON NANOTUBE; CHITOSAN; COLLAGEN; DIMETICONE; GELATIN; GOLD NANOPARTICLE; INDIUM TIN OXIDE; MEXILETINE; POLYESTER;

CARDIOTOXICITY; CELLS; ELASTICITY; ELECTRIC FIELD; ELECTROSTIMULATION; HEART; HEART FIBROBLAST; HEART MUSCLE CELL; HEART RIGHT VENTRICLE DYSPLASIA; HUMAN; HYDROGEL; IMMUNE RESPONSE; LEOPARD SYNDROME; NONHUMAN; REVIEW; TISSUE ENGINEERING; ANIMAL; BIOLOGICAL MODEL; CARDIAC MUSCLE CELL; CARDIOVASCULAR DISEASES; CELL CULTURE TECHNIQUE; CYTOLOGY; MATERIALS TESTING; PATHOPHYSIOLOGY; PHYSIOLOGY; PRECLINICAL STUDY; PROCEDURES; REGENERATIVE MEDICINE; TISSUE SCAFFOLD;

ANIMALS; BIOCOMPATIBLE MATERIALS; CARDIOVASCULAR DISEASES; CELL CULTURE TECHNIQUES; DRUG EVALUATION, PRECLINICAL; ELECTRIC STIMULATION; HEART; HUMANS; MATERIALS TESTING; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; POLYESTERS; REGENERATIVE MEDICINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84933039130     PISSN: 17486041     EISSN: 1748605X     Source Type: Journal    
DOI: 10.1088/1748-6041/10/3/034004     Document Type: Review

References (175)

1. Chiu L L and Radisic M 2011 Controlled release of thymosin beta4 using collagen-chitosan composite hydrogels promotes epicardial cell migration and angiogenesis J. Control. Release 155 376-85
2. Griffith L G and Naughton G 2002 Tissue engineering - current challenges and expanding opportunities Science 295 1009-14
3. Furth M E, Atala A and Van Dyke M E 2007 Smart biomaterials design for tissue engineering and regenerative medicine Biomaterials 28 5068-73
4. Franz S, Rammelt S, Scharnweber D and Simon J C 2011 Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials Biomaterials 32 6692-709
5. Bouten C V, Dankers P Y, Driessen-Mol A, Pedron S, Brizard A M and Baaijens F P 2011 Substrates for cardiovascular tissue engineering Adv. Drug Deliv. Rev. 63 221-41
6. Reis L A, Chiu L L, Feric N, Fu L and Radisic M 2014 Biomaterials in myocardial tissue engineering J. Tissue Eng. Regenerative Med. at press (doi: 10.1002/term.1944)
7. Zhao Y, Feric N T, Thavandiran N, Nunes S S and Radisic M 2014 The role of tissue engineering and biomaterials in cardiac regenerative medicine Can. J. Cardiol. 30 1307-22
8. Chen Q, Liang S and Thouas G A 2013 Elastomeric biomaterials for tissue engineering Prog. Polym. Sci. 38 584-671
9. Hirt M N, Hansen A and Eschenhagen T 2014 Cardiac tissue engineering: state of the art Circ. Res. 114 354-67
10. Zhang B, Xiao Y, Hsieh A, Thavandiran N and Radisic M 2011 Micro- and nanotechnology in cardiovascular tissue engineering Nanotechnology 22 494003
11. Ulery B D, Nair L S and Laurencin C T 2011 Biomedical applications of biodegradable polymers J. Polym. Sci. B Polym. Phys. 49 832-64
12. Chan B P and Leong K W 2008 Scaffolding in tissue engineering: general approaches and tissue-specific considerations Eur. Spine J. 17 467-79
13. Tian H, Tang Z, Zhuang X, Chen X and Jing X 2012 Biodegradable synthetic polymers: preparation, functionalization and biomedical application Prog. Polym. Sci. 37 237-80
14. Langer R and Tirrell D A 2004 Designing materials for biology and medicine Nature 428 487-92
15. Naderi H, Matin M M and Bahrami A R 2011 Review paper: critical issues in tissue engineering: biomaterials, cell sources, angiogenesis, and drug delivery systems J. Biomater. Appl. 26 383-417
16. Radisic M, Park H, Gerecht S, Cannizzaro C, Langer R and Vunjak-Novakovic G 2007 Biomimetic approach to cardiac tissue engineering Phil. Trans. R. Soc. B 362 1357-68
17. Nagueh S F et al 2004 Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy Circulation 110 155-62
18. Weis S M, Emery J L, Becker K D, McBride D J Jr, Omens J H and McCulloch A D 2000 Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim) Circ. Res. 87 663-9
19. Coirault C, Samuel J L, Chemla D, Pourney J C, Lambert F, Marotte F and Lecarpentier Y 1998 Increased compliance in diaphragm muscle of the cardiomyopathic Syrian hamster J. Appl. Physiol. 85 1762-9
20. Omens J H 1998 Stress and strain as regulators of myocardial growth Prog. Biophys. Mol. Biol. 69 559-72
21. Nelson D M, Ma Z, Fujimoto K L, Hashizume R and Wagner W R 2011 Intra-myocardial biomaterial injection therapy in the treatment of heart failure: materials, outcomes and challenges Acta Biomater. 7 1-15
22. Chuong C J, Sacks M S, Templeton G, Schwiep F and Johnson R L 1991 Regional deformation and contractile function in canine right ventricular free wall Am. J. Physiol. 260 H1224-35
23. Rappaport D, Adam D, Lysyansky P and Riesner S 2006 Assessment of myocardial regional strain and strain rate by tissue tracking in B-mode echocardiograms Ultrasound Med. Biol. 32 1181-92
24. Sacks M S and Chuong C J 1993 Biaxial mechanical properties of passive right ventricular free wall myocardium J. Biomech. Eng. 115 202-5
25. Engelmayr G C Jr, Cheng M, Bettinger C J, Borenstein J T, Langer R and Freed L E 2008 Accordion-like honeycombs for tissue engineering of cardiac anisotropy Nat. Mater. 7 1003-10
26. Holmes J W, Borg T K and Covell J W 2005 Structure and mechanics of healing myocardial infarcts Annu. Rev. Biomed. Eng. 7 223-53
27. Chuong C, Sacks M, Templeton G, Schwiep F and Johnson R 1991 Regional deformation and contractile function in canine right ventricular free wall Am. J. Physiol. Heart Circ. Physiol. 260 H1224-35
28. Demer L L and Yin F C 1983 Passive biaxial mechanical properties of isolated canine myocardium J. Physiol. 339 615-30
29. Fomovsky G M, Macadangdang J R, Ailawadi G and Holmes J W 2011 Model-based design of mechanical therapies for myocardial infarction J. Cardiovasc. Translational Res. 4 82-91
30. Fomovsky G M, Clark S A, Parker K M, Ailawadi G and Holmes J W 2012 Anisotropic reinforcement of acute anteroapical infarcts improves pump function Circ. Heart Fail. 5 515-22
31. Jawad H, Lyon A R, Harding S E, Ali N N and Boccaccini A R 2008 Myocardial tissue engineering Br. Med. Bull. 87 31-47
32. Anderson J M and Shive M S 2012 Biodegradation and biocompatibility of PLA and PLGA microspheres Adv. Drug Deliv. Rev. 64 72-82
33. Anderson J M 2001 Biological responses to materials Annu. Rev. Mater. Res. 31 81-110
34. Palmer J A, Abberton K M, Mitchell G M and Morrison W A 2014 Macrophage phenotype in response to implanted synthetic scaffolds: an immunohistochemical study in the rat Cells Tissues Organs 199 169-83
35. Anderson J M, Rodriguez A and Chang D T 2008 Foreign body reaction to biomaterials Semin. Immunol. 20 86-100
36. Montgomery M, Zhang B and Radisic M 2014 Cardiac tissue vascularization: from angiogenesis to microfluidic blood vessels J. Cardiovasc. Pharmacol. Ther. 19 382-93
37. Madden L R et al 2010 Proangiogenic scaffolds as functional templates for cardiac tissue engineering Proc. Natl Acad. Sci. USA 107 15211-6
38. Tran R T, Thevenot P, Gyawali D, Chiao J C, Tang L and Yang J 2010 Synthesis and characterization of a biodegradable elastomer featuring a dual crosslinking mechanism Soft Matter 6 2449-61
39. Zimmermann W H et al 2006 Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts Nat. Med. 12 452-8
40. Zimmermann W H et al 2006 Heart muscle engineering: an update on cardiac muscle replacement therapy Cardiovasc. Res. 71 419-29
41. Matsubayashi K, Fedak P W, Mickle D A, Weisel R D, Ozawa T and Li R K 2003 Improved left ventricular aneurysm repair with bioengineered vascular smooth muscle grafts Circulation 108 II-219-25
42. Kim D H et al 2012 Nanopatterned cardiac cell patches promote stem cell niche formation and myocardial regeneration Integrative Biol. 4 1019-33
43. Chi N H, Yang M C, Chung T W, Chou N K and Wang S S 2013 Cardiac repair using chitosan-hyaluronan/silk fibroin patches in a rat heart model with myocardial infarction Carbohydr. Polym. 92 591-7
44. Berry M F et al 2006 Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance Am. J. Physiol. Heart Circ. Physiol. 290 H2196-203
45. Tulloch N L et al 2011 Growth of engineered human myocardium with mechanical loading and vascular coculture Circ. Res. 109 47-59
46. Kehat I et al 2004 Electromechanical integration of cardiomyocytes derived from human embryonic stem cells Nat. Biotechnol. 22 1282-9
47. Gepstein L et al 2010 In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies Stem Cells 28 2151-61
48. Xue T et al 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 11-20
49. Shiba Y et al 2012 Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts Nature 489 322-5
50. Chong J J et al 2014 Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts Nature 510 273-7
51. Leor J, Amsalem Y and Cohen S 2005 Cells, scaffolds, and molecules for myocardial tissue engineering Pharmacol. Ther. 105 151-63
52. Prabhakaran M P, Venugopal J, Kai D and Ramakrishna S 2011 Biomimetic material strategies for cardiac tissue engineering Mater. Sci. Eng. C 31 503-13
53. Reis L A, Chiu L L, Liang Y, Hyunh K, Momen A and Radisic M 2012 A peptide-modified chitosan-collagen hydrogel for cardiac cell culture and delivery Acta Biomater. 8 1022-36
54. Leor J et al 2009 Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in swine J. Am. Coll. Cardiol. 54 1014-23
55. Landa N et al 2008 Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat Circulation 117 1388-96
56. Singelyn J M et al 2012 Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction J. Am. Coll. Cardiol. 59 751-63
57. Freytes D O, Stoner R M and Badylak S F 2008 Uniaxial and biaxial properties of terminally sterilized porcine urinary bladder matrix scaffolds J. Biomed. Mater. Res. B Appl. Biomater. 84 408-14
58. Ott H C et al 2008 Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart Nat. Med. 14 213-21
59. Singelyn J M, DeQuach J A, Seif-Naraghi S B, Littlefield R B, Schup-Magoffin P J and Christman K L 2009 Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering Biomaterials 30 5409-16
60. Sarig U et al 2012 Thick acellular heart extracellular matrix with inherent vasculature: a potential platform for myocardial tissue regeneration Tissue Eng. A 18 2125-37
61. Seif-Naraghi S B et al 2013 Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction Sci. Translational Med. 5 173ra25
62. Barrett D G and Yousaf M N 2010 Thermosets synthesized by thermal polyesterification for tissue engineering applications Soft Matter 6 5026
63. Burkersroda Fv, Schedl L and Göpferich A 2002 Why degradable polymers undergo surface erosion or bulk erosion Biomaterials 23 4221-31
64. Barrett D G, Luo W and Yousaf M N 2010 Aliphatic polyester elastomers derived from erythritol and α,ω-diacids Polym. Chem. 1 296
65. Vieira A C, Guedes R M and Marques A T 2009 Development of ligament tissue biodegradable devices: a review J. Biomech. 42 2421-30
66. Li Z and Guan J 2011 Hydrogels for cardiac tissue engineering Polymers 3 740-61
67. Vyner M C, Li A and Amsden B G 2014 The effect of poly(trimethylene carbonate) molecular weight on macrophage behavior and enzyme adsorption and conformation Biomaterials 35 9041-8
68. Li S 1999 Hydrolytic degradation characteristics of aliphatic polyesters derived from lactic and glycolic acids J. Biomed. Mater. Res. 48 342-53
69. Wang Y, Kim Y M and Langer R 2003 In vivo degradation characteristics of poly(glycerol sebacate) J. Biomed. Mater. Res. A 66A 192-7
70. Mukherjee S, Gualandi C, Focarete M L, Ravichandran R, Venugopal J R, Raghunath M and Ramakrishna S 2011 Elastomeric electrospun scaffolds of poly(J. Mater. Sci. Mat. Med. 22 1689-99
71. Nelson D M, Hashizume R, Yoshizumi T, Blakney A K, Ma Z and Wagner W R 2014 Intramyocardial injection of a synthetic hydrogel with delivery of bFGF and IGF1 in a rat model of ischemic cardiomyopathy Biomacromolecules 15 1-11
72. Hoshi R A, Behl S and Ameer G A 2009 Nanoporous biodegradable elastomers Adv. Mater. 21 188-92
73. Pahnke A, Montgomery M and Radisic M 2015 Spatial and electrical factors regulating cardiac regeneration and assembly Biomaterials for Cardiac Regeneration (Cham: Springer) pp 71-92
74. Jawad H, Ali N N, Lyon A R, Chen Q Z, Harding S E and Boccaccini A R 2007 Myocardial tissue engineering: a review J. Tissue Eng. Regenerative Med. 1 327-42
75. Lian X et al 2012 Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling Proc. Natl Acad. Sci. USA 109 E1848-57
76. Takahashi K et al 2007 Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 861-72
77. Sanganalmath S K and Bolli R 2013 Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions Circ. Res. 113 810-34
78. Lipinski M J et al 2007 Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials J. Am. Coll. Cardiol. 50 1761-7
79. Nowbar A N et al 2014 Discrepancies in autologous bone marrow stem cell trials and enhancement of ejection fraction (DAMASCENE): weighted regression and meta-analysis BMJ 348 g2688
80. Clifford D M, Fisher S A, Brunskill S J, Doree C, Mathur A, Watt S and Martin-Rendon E 2012 Stem cell treatment for acute myocardial infarction Cochrane Database Syst. Rev. 2 CD006536
81. Qian L et al 2012 In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes Nature 485 593-8
82. Song K et al 2012 Heart repair by reprogramming non-myocytes with cardiac transcription factors Nature 485 599-604
83. Nam Y-J et al 2013 Reprogramming of human fibroblasts toward a cardiac fate Proc. Natl Acad. Sci. USA 110 5588-93
84. Qian L, Berry E C, Fu J D, Ieda M and Srivastava D 2013 Reprogramming of mouse fibroblasts into cardiomyocyte-like cells in vitro Nat. Protocols 8 1204-15
85. Brutsaert D L 2003 Cardiac endothelial-myocardial signaling: its role in cardiac growth, contractile performance, and rhythmicity Physiol. Rev. 83 59-115
86. Brutsaert D L, Fransen P, Andries L J, De Keulenaer G W and Sys S U 1998 Cardiac endothelium and myocardial function Cardiovasc. Res. 38 281-90
87. Giordano F J et al 2001 A cardiac myocyte vascular endothelial growth factor paracrine pathway is required to maintain cardiac function Proc. Natl Acad. Sci. USA 98 5780-5
88. Narmoneva D A, Vukmirovic R, Davis M E, Kamm R D and Lee R T 2004 Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration Circulation 110 962-8
89. Chiu L L, Montgomery M, Liang Y, Liu H and Radisic M 2012 Perfusable branching microvessel bed for vascularization of engineered tissues Proc. Natl Acad. Sci. USA 109 E3414-23
90. MacKenna D, Summerour S R and Villarreal F J 2000 Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis Cardiovasc. Res. 46 257-63
91. Baudino T A, Carver W, Giles W and Borg T K 2006 Cardiac fibroblasts: friend or foe? Am. J. Physiol. Heart Circ. Physiol. 291 H1015-26
92. Banerjee I, Yekkala K, Borg T K and Baudino T A 2006 Dynamic interactions between myocytes, fibroblasts, and extracellular matrix Ann. NY Acad. Sci. 1080 76-84
93. Iyer R K, Chiu L L and Radisic M 2009 Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering J. Biomed. Mater. Res. A 89 616-31
94. Iyer R K, Odedra D, Chiu L L, Vunjak-Novakovic G and Radisic M 2012 Vascular endothelial growth factor secretion by nonmyocytes modulates Connexin-43 levels in cardiac organoids Tissue Eng. A 18 1771-83
95. Thavandiran N et al 2013 Design and formulation of functional pluripotent stem cell-derived cardiac microtissues Proc. Natl Acad. Sci. USA 110 E4698-707
96. Caspi O et al 2009 In vitro electrophysiological drug testing using human embryonic stem cell derived cardiomyocytes Stem Cells Dev. 18 161-72
97. Itzhaki I et al 2011 Modelling the long QT syndrome with induced pluripotent stem cells Nature 471 225-9
98. Liang P et al 2013 Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity Circulation 127 1677-91
99. Karp J M et al 2006 A photolithographic method to create cellular micropatterns Biomaterials 27 4755-64
100. Badie N and Bursac N 2009 Novel micropatterned cardiac cell cultures with realistic ventricular microstructure Biophys. J. 96 3873-85
101. Guo L et al 2011 Estimating the risk of drug-induced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes Toxicol. Sci. 123 281-9
102. Guo L, Coyle L, Abrams R M, Kemper R, Chiao E T and Kolaja K L 2013 Refining the human iPSC-cardiomyocyte arrhythmic risk assessment model Toxicol. Sci. 136 581-94
103. Lamore S D, Kamendi H W, Scott C W, Dragan Y P and Peters M F 2013 Cellular impedance assays for predictive preclinical drug screening of kinase inhibitor cardiovascular toxicity Toxicol. Sci. 135 402-13
104. Natarajan A et al 2011 Patterned cardiomyocytes on microelectrode arrays as a functional, high information content drug screening platform Biomaterials 32 4267-74
105. Wang J et al 2013 Effect of engineered anisotropy on the susceptibility of human pluripotent stem cell-derived ventricular cardiomyocytes to arrhythmias Biomaterials 34 8878-86
106. Chen A et al 2014 Integrated platform for functional monitoring of biomimetic heart sheets derived from human pluripotent stem cells Biomaterials 35 675-83
107. Grosberg A, Alford P W, McCain M L and Parker K K 2011 Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip Lab Chip 11 4165-73
108. Song H, Zandstra P W and Radisic M 2011 Engineered heart tissue model of diabetic myocardium Tissue Eng. A 17 1869-78
109. Ma Z et al 2014 3D filamentous human diseased cardiac tissue model Biomaterials 35 1367-77
110. Baar K, Birla R, Boluyt M O, Borschel G H, Arruda E M and Dennis R G 2005 Self-organization of rat cardiac cells into contractile 3D cardiac tissue FASEB J. 19 275-7
111. Barocas V H and Tranquillo R T 1997 An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance J. Biomech. Eng. 119 137-45
112. Schaaf S et al 2011 Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology PloS One 6 e26397
113. Ramade A, Legant W R, Picart C, Chen C S and Boudou T 2014 Microfabrication of a platform to measure and manipulate the mechanics of engineered microtissues Methods Cell Biol. 121 191-211
114. Nunes S S et al 2013 Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes Nat. Methods 10 781-7
115. Xiao Y et al 2013 Microfabricated perfusable cardiac biowire: a platform that mimics native cardiac bundle Lab Chip 14 869-82
116. Yang X, Pabon L and Murry C E 2014 Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes Circ. Res. 114 511-23
117. Tandon N et al 2009 Electrical stimulation systems for cardiac tissue engineering Nat. Protocols 4 155-73
118. Radisic M et al 2004 Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds Proc. Natl Acad. Sci. USA 101 18129-34
119. Lasher R A, Pahnke A Q, Johnson J M, Sachse F B and Hitchcock R W 2012 Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype J. Tissue Eng. 3 2041731412455354
120. Chiu L L Y, Iyer R K, King J-P and Radisic M 2011 Biphasic electrical field stimulation aids in tissue engineering of multicell-type cardiac organoids Tissue Eng. A 17 1465-77
121. Tung L and Borderies J R 1992 Analysis of electric field stimulation of single cardiac muscle cells Biophys. J. 63 371-86
122. Liau B, Zhang D and Bursac N 2012 Functional cardiac tissue engineering Regenerative Med. 7 187-206
123. Kai D, Prabhakaran M P, Jin G and Ramakrishna S 2011 Polypyrrole-contained electrospun conductive nanofibrous membranes for cardiac tissue engineering J. Biomed. Mater. Res. A 99 376-85
124. Fleischer S, Shevach M, Feiner R and Dvir T 2014 Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues Nanoscale 6 9410-4
125. Dvir T et al 2011 Nanowired 3D cardiac patches Nat. Nanotechnol. 6 720-5
126. Shin S R et al 2013 Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators ACS Nano 7 2369-80
127. Mooney E et al 2012 The electrical stimulation of carbon nanotubes to provide a cardiomimetic cue to MSCs Biomaterials 33 6132-9
128. Martins A M, Eng G, Caridade S G, Mano J F, Reis R L and Vunjak-Novakovic G 2014 Electrically conductive chitosan/carbon scaffolds for cardiac tissue engineering Biomacromolecules 15 635-43
129. Rajabi M, Kassiotis C, Razeghi P and Taegtmeyer H 2007 Return to the fetal gene program protects the stressed heart: a strong hypothesis Heart Fail. Rev. 12 331-43
130. Ahadian S et al 2013 Electrical stimulation as a biomimicry tool for regulating muscle cell behavior Organogenesis 9 87-92
131. Chan Y C et al 2013 Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells J. Cardiovasc. Translational Res. 6 989-99
132. Sukardi H, Chng H T, Chan E C, Gong Z and Lam S H 2011 Zebrafish for drug toxicity screening: bridging the in vitro cell-based models and in vivo mammalian models Expert Opin. Drug Metab Toxicol. 7 579-89
133. Mullard A 2014 New drugs cost US $2.6 billion to develop Nat. Rev. Drug Discov. 13 877
134. Dykens J A, Marroquin L D and Will Y 2007 Strategies to reduce late-stage drug attrition due to mitochondrial toxicity Expert Rev. Mol. Diagn. 7 161-75
135. Piccini J P et al 2009 Current challenges in the evaluation of cardiac safety during drug development: translational medicine meets the critical path initiative Am. Heart J. 158 317-26
136. Chen M X et al 2007 Improved functional expression of recombinant human ether-a-go-go (hERG) K+ channels by cultivation at reduced temperature BMC Biotechnol. 7 93
137. Moretti A et al 2010 Patient-specific induced pluripotent stem-cell models for long-QT syndrome New Engl. J. Med. 363 1397-409
138. Mahajan A et al 2008 Modifying L-type calcium current kinetics: consequences for cardiac excitation and arrhythmia dynamics Biophys. J. 94 411-23
139. Will Y et al 2008 Effect of the multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib, and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells Toxicol. Sci. 106 153-61
140. Marroquin L D, Hynes J, Dykens J A, Jamieson J D and Will Y 2007 Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants Toxicol. Sci. 97 539-47
141. Mellor H R, Bell A R, Valentin J P and Roberts R R 2011 Cardiotoxicity associated with targeting kinase pathways in cancer Toxicol. Sci. 120 14-32
142. Braam S R, Tertoolen L, van de Stolpe A, Meyer T, Passier R and Mummery C L 2010 Prediction of drug-induced cardiotoxicity using human embryonic stem cell-derived cardiomyocytes Stem Cell Res. 4 107-16
143. Clements M and Thomas N 2014 High-throughput multi-parameter profiling of electrophysiological drug effects in human embryonic stem cell derived cardiomyocytes using multi-electrode arrays Toxicol Sci. 140 445-61
144. Kaneko T et al 2014 On-chip in vitro cell-network pre-clinical cardiac toxicity using spatiotemporal human cardiomyocyte measurement on a chip Sci. Rep. 4 4670
145. Kehat I, Gepstein A, Spira A, Itskovitz-Eldor J and Gepstein L 2002 High-resolution electrophysiological assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction Circ. Res. 91 659-61
146. Gessert S and Kuhl M 2010 The multiple phases and faces of wnt signaling during cardiac differentiation and development Circ. Res. 107 186-99
147. Liang G, Guvanasen G S, Xi L, Tuthill C, Nichols T R and DeWeerth S P 2013 A PDMS-based integrated stretchable microelectrode array (isMEA) for neural and muscular surface interfacing IEEE Trans. Biomed. Circuits Syst. 7 1-10
148. Tandon N et al 2010 Surface-patterned electrode bioreactor for electrical stimulation Lab Chip 10 692-700
149. Takebe T et al 2013 Vascularized and functional human liver from an iPSC-derived organ bud transplant Nature 499 481-4
150. Yulin X, Lizhen L, Lifei Z, Shan F, Ru L, Kaimin H and Huang H 2012 Efficient generation of induced pluripotent stem cells from human bone marrow mesenchymal stem cells Folia Biol. (Praha) 58 221-30
151. Frobel J et al 2014 Epigenetic rejuvenation of mesenchymal stromal cells derived from induced pluripotent stem cells Stem Cell Rep. 3 414-22
152. Zwi-Dantsis L et al 2013 Derivation and cardiomyocyte differentiation of induced pluripotent stem cells from heart failure patients Eur. Heart J. 34 1575-86
153. Levine E, Rosero S Z, Budzikowski A S, Moss A J, Zareba W and Daubert J P 2008 Congenital long QT syndrome: considerations for primary care physicians Cleve Clin. J. Med. 75 591-600
154. Ma D et al 2013 Modeling type 3 long QT syndrome with cardiomyocytes derived from patient-specific induced pluripotent stem cells Int. J. Cardiol. 168 5277-86
155. Yazawa M et al 2011 Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome Nature 471 230-4
156. Carvajal-Vergara X et al 2010 Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome Nature 465 808-12
157. Sun N et al 2012 Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy Sci. Transl. Med. 4 130ra47
158. Wang G et al 2014 Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies Nat. Med. 20 616-23
159. Kim C et al 2013 Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs Nature 494 105-10
160. Chitcholtan K, Asselin E, Parent S, Sykes P H and Evans J J 2013 Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer Exp. Cell Res. 319 75-87
161. Bellis A D et al 2013 Dynamic transcription factor activity profiling in 2D and 3D cell cultures Biotechnol. Bioeng. 110 563-72
162. Maltman D J and Przyborski S A 2010 Developments in 3D cell culture technology aimed at improving the accuracy of in vitro analyses Biochem. Soc. Trans. 38 1072-5
163. Lovitt C J, Shelper T B and Avery V M 2014 Advanced cell culture techniques for cancer drug discovery Biology 3 345-67
164. Radisic M, Euloth M, Yang L, Langer R, Freed L E and Vunjak-Novakovic G 2003 High-density seeding of myocyte cells for cardiac tissue engineering Biotechnol. Bioeng. 82 403-14
165. Boudou T et al 2012 A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues Tissue Eng. A 18 910-9
166. Riegler J, Gillich A, Shen Q, Gold J D and Wu J C 2014 Cardiac tissue slice transplantation as a model to assess tissue-engineered graft thickness, survival, and function Circulation 130 S77-86
167. Zimmermann W H et al 2002 Tissue engineering of a differentiated cardiac muscle construct Circ. Res. 90 223-30
168. Sniadecki N J and Chen C S 2007 Microfabricated silicone elastomeric post arrays for measuring traction forces of adherent cells Methods Cell Biol. 83 313-28
169. Eschenhagen T, Zimmermann W H and Kleber A G 2006 Electrical coupling of cardiac myocyte cell sheets to the heart Circ. Res. 98 573-5
170. Maeda H, Ohashi E, Sano A, Kawasaki H and Kurosaki Y 2003 Investigation of the release behavior of a covered-rod-type formulation using silicone J. Control. Release 90 59-70
171. Lee J H, Pidaparti R M, Atkinson G M and Moorthy R S 2012 Design of an implantable device for ocular drug delivery J. Drug Deliv. 2012 527516
172. Kimura T 1985 Studies on the clinical application of medical grade silicone rubber to maxillofacial prosthetics - bacteriological analysis of the surface adherent substance and the prevention of its attachment Kokubyo Gakkai Zasshi 52 558-86
173. Johnston I D, McCluskey D K, Tan C K L and Tracey M C 2014 Mechanical characterization of bulk Sylgard 184 for microfluidics and microengineering J. Micromech. Microeng. 24 035017
174. Marsano A et al 2010 Scaffold stiffness affects the contractile function of 3D engineered cardiac constructs Biotechnol. Prog. 26 1382-90
175. Domansky K et al 2013 Clear castable polyurethane elastomer for fabrication of microfluidic devices Lab Chip 13 3956-64