Characterizing functional stem cell-cardiomyocyte interactions

Regenerative Medicine

Volumn 5, Issue 1, 2010, Pages 87-105

  Bursac, Nenad ^a   Kirkton, Robert D ^a   McSpadden, Luke C ^a   Liau, Brian ^a  

^a Duke University   (United States)

Author keywords

Arrhythmia; Cellular cardiomyoplasty; Co culture; Contractile force; Micropatterning; Stem cells

Indexed keywords

CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL MIGRATION; GRAFT SURVIVAL; HEART ARRHYTHMIA; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE ISCHEMIA; HUMAN; NONHUMAN; PATIENT SAFETY; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; THERAPY EFFECT;

CELL COMMUNICATION; HEART FAILURE; METHODS; MYOCYTES, CARDIAC; STEM CELLS;

EID: 77649331404     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/rme.09.69     Document Type: Review

References (116)

1. Rosamond W, Flegal K, Furie K et al.: Heart Disease and Stroke Statistics-2008 Update. A Report From the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 117, e25-e146 (2008).
2. Marelli D, Desrosiers C, El-Alfy M, Kao RL, Chiu RC: Cell transplantation for myocardial repair: an experimental approach. Cell Transplant. 1(6), 383-390 (1992).
3. Koh GY, Klug MG, Soonpaa MH, Field LJ: Differentiation and long-term survival of c2c12 myoblast grafts in heart. J. Clin. Invest. 92(3), 1548-1554 (1993).
4. Menasche P, Alfieri O, Janssens S et al.: The myoblast autologous grafting in ischemic cardiomyopathy (magic) trial. First randomized placebo-controlled study of myoblast transplantation. Circulation 117(9), 1189-1200 (2008).
5. Haider H, Lei Y, Ashraf M: Myocell, a cell-based, autologous skeletal myoblast therapy for the treatment of cardiovascular diseases. Curr. Opin. Mol. Ther. 10(6), 611-621 (2008).
6. Singh S, Arora R, Handa K et al..: Stem cells improve left ventricular function in acute myocardial infarction. Clin. Cardiol. 32(4), 176-180 (2009).
7. Dill T, Schachinger V, Rolf A et al..: Intracoronary administration of bone marrow-derived progenitor cells improves left ventricular function in patients at risk for adverse remodeling after acute ST-segment elevation myocardial infarction: results of the reinfusion of enriched progenitor cells and infarct remodeling in acute myocardial infarction study (REPAIR-AMI) cardiac magnetic resonance imaging substudy. Am. Heart J. 157(3), 541-547 (2009).
8. Losordo DW, Schatz RA, White CJ et al.: Intramyocardial transplantation of autologous CD34 stem cells for intractable angina: a Phase I/IIA double-blind, randomized controlled trial. Circulation 115(25), 3165-3172 (2007).
9. Tatsumi T, Ashihara E, Yasui T et al.: Intracoronary transplantation of non-expanded peripheral blood-derived mononuclear cells promotes improvement of cardiac function in patients with acute myocardial infarction. Circ. J. 71(8), 1199-1207 (2007).
10. Smith RR, Barile L, Cho HC et al.: Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7), 896-908 (2007).
11. Bearzi C, Rota M, Hosoda T et al.: Human cardiac stem cells. Proc. Natl Acad. Sci. USA 104(35), 14068-14073 (2007).
12. Gnecchi M, Zhang Z, Ni A, Dzau VJ: Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 103(11), 1204-1219 (2008).
13. Burchfield JS, Dimmeler S: Role of paracrine factors in stem and progenitor cell mediated cardiac repair and tissue fibrosis. Fibrogenesis Tissue Repair 1(1), 4 (2008).
14. Mazhari R, Hare JM: Mechanisms of action of mesenchymal stem cells in cardiac repair: Potential influences on the cardiac stem cell niche. Nat. Clin. Pract. Cardiovasc. Med. 4(Suppl. 1), S21-S26 (2007).
15. Laflamme MA, Murry CE: Regenerating the heart. Nat. Biotechnol. 23(7), 845-856 (2005).
16. 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).
17. Mauritz C, Schwanke K, Reppel M et al.: Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118(5), 507-517 (2008).
18. Li H, Yu B, Zhang Y, Pan Z, Xu W, Li H: Jagged1 protein enhances the differentiation of mesenchymal stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 341(2), 320-325 (2006). (Pubitemid 43152109)
19. Boni A, Urbanek K, Nascimbene A et al.: Notch1 regulates the fate of cardiac progenitor cells. Proc. Natl Acad. Sci. USA 105(40), 15529-15534 (2008).
20. Roell W, Lewalter T, Sasse P et al.: Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia. Nature 450(7171), 819-824 (2007).
21. Mills WR, Mal N, Kiedrowski MJ et al.: Stem cell therapy enhances electrical viability in myocardial infarction. J. Mol. Cell. Cardiol. 42(2), 304-314 (2007).
22. Crisostomo PR, Abarbanell AM, Wang M, Lahm T, Wang Y, Meldrum DR: Embryonic stem cells attenuate myocardial dysfunction and inflammation after surgical global ischemia via paracrine actions. Am. J. Physiol. Heart Circ. Physiol. 295(4), H1726-H1735 (2008).
23. Kraitchman DL, Heldman AW, Atalar E et al..: In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 107(18), 2290-2293 (2003).
24. Cao F, Lin S, Xie X et al.: In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 113(7), 1005-1014 (2006).
25. Shen D, Liu D, Cao Z, Acton PD, Zhou R: Coregistration of magnetic resonance and single photon emission computed tomography images for noninvasive localization of stem cells grafted in the infarcted rat myocardium. Mol. Imaging Biol. 9(1), 24-31 (2007).
26. Amsalem Y, Mardor Y, Feinberg MS et al.: Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116(Suppl. 11), I38-I45 (2007).
27. Hofmann M, Wollert KC, Meyer GP et al.: Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111(17), 2198-2202 (2005).
28. Zhou R, Acton PD, Ferrari VA: Imaging stem cells implanted in infarcted myocardium. J. Am. Coll. Cardiol. 48(10), 2094-2106 (2006).
29. Nyolczas N, Charwat S, Posa A et al.: Tracking the migration of cardially delivered therapeutic stem cells in vivo: state of the art. Regen. Med. 4(3), 407-422 (2009).
30. Ramanathan C, Jia P, Ghanem R, Ryu K, Rudy Y: Activation and repolarization of the normal human heart under complete physiological conditions. Proc. Natl Acad. Sci. USA 103(16), 6309-6314 (2006).
31. Amado LC, Schuleri KH, Saliaris AP et al.: Multimodality noninvasive imaging demonstrates in vivo cardiac regeneration after mesenchymal stem cell therapy. J. Am. Coll. Cardiol. 48(10), 2116-2124 (2006).
32. Li Z, Lee A, Huang M et al.: Imaging survival and function of transplanted cardiac resident stem cells. J. Am. Coll. Cardiol. 53(14), 1229-1240 (2009).
33. Anversa P, Leri A, Rota M et al.: Concise review: stem cells, myocardial regeneration, and methodological artifacts. Stem Cells 25(3), 589-601 (2007).
34. Rubart M, Pasumarthi KB, Nakajima H, Soonpaa MH, Nakajima HO, Field LJ: Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ. Res. 92(11), 1217-1224 (2003).
35. Rota M, Kajstura J, Hosoda T et al..: Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc. Natl Acad. Sci. USA 104(45), 17783-17788 (2007).
36. Aistrup GL, Kelly JE, Kapur S et al.: Pacing-induced heterogeneities in intracellular Ca2 signaling, cardiac alternans, and ventricular arrhythmias in intact rat heart. Circ. Res. 99(7), e65-e73 (2006).
37. Fujiwara K, Tanaka H, Mani H, Nakagami T, Takamatsu T: Burst emergence of intracellular Ca2 waves evokes arrhythmogenic oscillatory depolarization via the Na+-Ca2+ exchanger: simultaneous confocal recording of membrane potential and intracellular Ca2+ in the heart. Circ. Res. 103(5), 509-518 (2008).
38. Fedorov VV, Lozinsky IT, Sosunov EA et al.: Application of blebbistatin as an excitation- contraction uncoupler for electrophysiologic study of rat and rabbit hearts. Heart Rhythm 4(5), 619-626 (2007).
39. Rubart M, Soonpaa MH, Nakajima H, Field LJ: Spontaneous and evoked intracellular calcium transients in donor-derived myocytes following intracardiac myoblast transplantation. J. Clin. Invest. 114(6), 775-783 (2004).
40. Rubart M: Two-photon microscopy of cells and tissue. Circ. Res. 95(12), 1154-1166 (2004).
41. Aistrup GL, Shiferaw Y, Kapur S, Kadish AH, Wasserstrom JA: Mechanisms underlying the formation and dynamics of subcellular calcium alternans in the intact rat heart. Circ. Res. 104(5), 639-649 (2009).
42. Kleber A, Rudy Y: Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol. Rev. 84(2), 431-488 (2004).
43. Efimov IR, Nikolski VP, Salama G: Optical imaging of the heart. Circ. Res. 95(1), 21-33 (2004).
44. Salama G, Hwang SM: Simultaneous optical mapping of intracellular free calcium and action potentials from Langendorff perfused hearts. Curr. Protoc. Cytom. Chapter 12, Unit 12,17 (2009).
45. Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF: Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J. Neurosci. 28(29), 7399-7411 (2008).
46. Mao T, O'Connor DH, Scheuss V, Nakai J, Svoboda K: Characterization and subcellular targeting of gcamp-type genetically-encoded calcium indicators. PloS ONE 3(3), e1796 (2008).
47. Fletcher ML, Masurkar AV, Xing J et al.: Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb. J. Neurophysiol. 102, 817-830 (2009).
48. Lee MY, Song H, Nakai J et al.: Local subplasma membrane Ca2 signals detected by a tethered Ca2 sensor. Proc. Natl Acad. Sci. USA 103(35), 13232-13237 (2006).
49. Tallini YN, Ohkura M, Choi BR et al..: Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2 indicator gcamp2. Proc. Natl Acad. Sci. USA 103(12), 4753-4758 (2006).
50. Tallini YN, Brekke JF, Shui B et al.: Propagated endothelial Ca2 waves and arteriolar dilation in vivo: measurements in cx40bac gCaMP2 transgenic mice. Circ. Res. 101(12), 1300-1309 (2007).
51. Kehat I, Gepstein A, Spira A, Itskovitz-Eldor J, Gepstein L: High-resolution electrophysiological assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ. Res. 91, 659-661 (2002).
52. Zhang J, Wilson GF, Soerens AG et al.: Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ. Res. 104(4), e30-41 (2009).
53. Freund C, Mummery CL: Prospects for pluripotent stem cell-derived cardiomyocytes in cardiac cell therapy and as disease models. J. Cell. Biochem. 107(4), 592-599 (2009).
54. Winter E, Grauss R, Hogers B et al.: Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation 116, 917-927 (2007).
55. Kruithof B, van Wijk B, Somi S et al..: BMP and FGF regulate the differentiation of mulipotential pericardial mesoderm into the myocardial or epicardial lineage. Dev. Biol. 295, 507-522 (2006).
56. Bai X, Pinkernell K, Song Y, Nabzdyk C, Reiser J, Alt E: Genetically selected stem cells from human adipose tissue express cardiac markers. Biochem. Biophys. Res. Commun. 353, 665-671 (2007).
57. Fraser J, Schreiber R, Strem B et al..: Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat. Clin. Pract. Cardiovasc. Med. 3(Suppl. 1), S33-S37 (2006).
58. Muller-Borer B, Cascio W, Esch G et al..: Mechanisms controlling the acquisition of a cardiac phenotype by liver stem cells. Proc. Natl Acad. Sci. USA 104, 3877-3882 (2007). (Pubitemid 47181547)
59. Kogler G, Sensken S, Airey J et al..: A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J. Exp. Med. 200, 123-135 (2004).
60. Chiavegato A, Bollini S, Pozzobon M et al..: Human amniotic fluid-derived stem cells are rejected after transplantation in the myocardium of normal, ischemic, immuno-suppressed or immuno-deficient rats. J. Mol. Cell. Cardiol. 42, 746-759 (2007).
61. Sartore S, Lenzi M, Angelini A et al.: Amniotic mesenchymal cells autotransplanted in a porcine model of cardiac ischemia do not differentiate to cardiogenic phenotypes. Eur. J. Cardiothorac. Surg. 28, 677-684 (2005).
62. Falconnet D, Csucs G, Grandin HM, Textor M: Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials 27(16), 3044-3063 (2006).
63. Badie N, Bursac N: Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. Biophys. J. 96(9), 3873-3885 (2009).
64. Rohr S, Sholly D, Kleber A: Patterned growth of neonatal rat heart cells in culture: morphological and electrophysiological characterization. Circ. Res. 68, 114-130 (1991).
65. Gaudesius G, Miragoli M, Thomas SP, Rohr S: Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ. Res. 93(5), 421-428 (2003).
66. Derksen R, van Rijen HV, Wilders R et al.: Tissue discontinuities affect conduction velocity restitution: a mechanism by which structural barriers may promote wave break. Circulation 108(7), 882-888 (2003).
67. Bursac N, Tung L: Acceleration of functional reentry by rapid pacing in anisotropic cardiac monolayers: formation of multi-wave functional reentries. Cardiovasc. Res. 69(2), 381-390 (2006).
68. Fast V, Cheek ER, Pollard AE, Ideker RE: Effects of electrical shocks on CAi2 and VM in myocyte cultures. Circulation Res. 94(12), 1589-1597 (2004).
69. Pedrotty DM, Klinger RY, Badie N, Hinds S, Kardashian A, Bursac N: Structural coupling of cardiomyocytes and noncardiomyocytes: quantitative comparisons using a novel micropatterned cell pair assay. Am. J. Physiol. Heart Circ. Physiol. 295(1), H390-H400 (2008).
70. Wade M, Trosko J, Schindler M: Fluorescence photobleaching assay of gap junction-mediated communication between human cells. Science 232, 525-528 (1986).
71. Abbaci M, Barberi-Heyob M, Stines J et al.: Gap junctional intercellular communication capacity by gap-frap technique: a comparative study. Biotechnol. J. 2, 50-61 (2007).
72. Valiunas V, Doronin S, Valiuniene L et al.: Human mesenchymal stem cells make cardiac connexins and form functional gap junctions. J. Physiol. 555(Pt 3), 617-626 (2004).
73. Del Corsso C, Srinivas M, Urban-Maldonado M et al..: Transfection of mammalian cells with connexins and measurement of voltage sensitivity of their gap junctions. Nat. Protoc. 1(4), 1799 - 1809 (2006).
74. van Rijen HV, Wilders R, Rook MB, Jongsma HJ: Dual patch clamp. Methods Mol. Biol. 154, 269-292 (2001).
75. Klinger R, Bursac N: Cardiac cell therapy in vitro: reproducible assays for comparing the efficacy of different donor cells. IEEE Eng. Med. Biol. Mag. 27(1), 72-80 (2008).
76. Pijnappels D, Van Tuyn J, De Vries A et al.: Resynchronization of separated rat cardiomyocytes fields with genetically modified human ventricular scar fibroblasts. Circulation 116, 2018-2028 (2007).
77. Kondratyev AA, Ponard JG, Munteanu A, Rohr S, Kucera JP: Dynamic changes of cardiac conduction during rapid pacing. Am. J. Physiol. Heart Circ. Physiol. 292(4), H1796-H1811 (2007).
78. Miragoli M, Gaudesius G, Rohr S: Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circ. Res. 98(6), 801-810 (2006).
79. Pijnappels DA, Schalij MJ, Ramkisoensing AA et al.: Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ. Res. 103(2), 167-176 (2008).
80. Beeres SL, Atsma DE, van Der Laarse A et al..: Human adult bone marrow mesenchymal stem cells repair experimental conduction block in rat cardiomyocyte cultures. J. Am. Coll. Cardiol. 46(10), 1943-1952 (2005).
81. Folch A, Jo BH, Hurtado O, Beebe DJ, Toner M: Microfabricated elastomeric stencils for micropatterning cell cultures. J. Biomed. Mater. Res. 52(2), 346-353 (2000).
82. Bursac N, Aguel F, Tung L: Multiarm spirals in a two-dimensional cardiac substrate. Proc. Natl Acad. Sci. USA 101(43), 15530-15534 (2004).
83. Munoz V, Grzeda KR, Desplantez T et al..: Adenoviral expression of iks contributes to wavebreak and fibrillatory conduction in neonatal rat ventricular cardiomyocyte monolayers. Circ. Res. 101(5), 475-483 (2007).
84. De Diego C, Pai RK, Chen F et al.: Electrophysiological consequences of acute regional ischemia/reperfusion in neonatal rat ventricular myocyte monolayers. Circulation 118(23), 2330-2337 (2008).
85. Ferrick KJ, Maher M, Roth JA, Kim SG, Fisher JD: Reproducibility of electrophysiological testing during antiarrhythmic therapy for ventricular arrhythmias unrelated to coronary artery disease. Pacing Clin. Electrophysiol. 18(7), 1395-1400 (1995).
86. Liu J, Fu JD, Siu CW, Li RA: Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 25(12), 3038-3044 (2007).
87. Satin J, Itzhaki I, Rapoport S et al..: Calcium handling in human embryonic stem cell-derived cardiomyocytes. Stem Cells 26(8), 1961-1972 (2008).
88. Zlochiver S, Munoz V, Vikstrom KL, Taffet SM, Berenfeld O, Jalife J: Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophys. J. 95(9), 4469-4480 (2008).
89. Chang MG, Tung L, Sekar RB et al.: Proarrhythmic potential of mesenchymal stem cell transplantation revealed in an in vitro coculture model. Circulation 113(15), 1832-1841 (2006).
90. Abraham MR, Henrikson CA, Tung L et al.: Antiarrhythmic engineering of skeletal myoblasts for cardiac transplantation. Circ. Res. 97(2), 159-167 (2005).
91. Valderrabano M: Influence of anisotropic conduction properties in the propagation of the cardiac action potential. Prog. Biophys. Mol. Biol. 94(1-2), 144-168 (2007).
92. Plotnikov AN, Shlapakova I, Szabolcs MJ et al.: Xenografted adult human mesenchymal stem cells provide a platform for sustained biological pacemaker function in canine heart. Circulation 116(7), 706-713 (2007).
93. Xue T, Cho HC, Akar FG et al.: Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 111(1), 11-20 (2005).
94. 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). (Pubitemid 39341201)
95. Orlic D, Kajstura J, Chimenti S et al.: Bone marrow cells regenerate infarcted myocardium. Nature 410(6829), 701-705 (2001).
96. Kohl P, Camelliti P: Cardiac myocyte-nonmyocyte electrotonic coupling: Implications for ventricular arrhythmogenesis. Heart Rhythm 4(2), 233-235 (2007).
97. Mcspadden LC, Kirkton RD, Bursac N: Electrotonic loading of anisotropic cardiac monolayers by unexcitable cells depends on connexin type and expression level. Am. J. Physiol. Cell Physiol. 297, C339-C351 (2009).
98. Miragoli M, Salvarani N, Rohr S: Myofibroblasts induce ectopic activity in cardiac tissue. Circ. Res. 101(8), 755-758 (2007).
99. Feld Y, Melamed-Frank M, Kehat I, Tal D, Marom S, Gepstein L: Electrophysiological modulation of cardiomyocytic tissue by transfected fibroblasts expressing potassium channels: a novel strategy to manipulate excitability. Circulation 105(4), 522-529 (2002).
100. Fahrenbach JP, Ai X, Banach K: Decreased intercellular coupling improves the function of cardiac pacemakers derived from mouse embryonic stem cells. J. Mol. Cell. Cardiol. 45(5), 642-649 (2008).
101. Pillekamp F, Reppel M, Dinkelacker V et al..: Establishment and characterization of a mouse embryonic heart slice preparation. Cell. Physiol. Biochem. 16(1-3), 127-132 (2005).
102. Pillekamp F, Reppel M, Rubenchyk O et al.: Force measurements of human embryonic stem cell-derived cardiomyocytes in an in vitro transplantation model. Stem Cells 25(1), 174-180 (2007).
103. Habeler W, Pouillot S, Plancheron A, Puceat M, Peschanski M, Monville C: An in vitro beating heart model for long-term assessment of experimental therapeutics. Cardiovasc. Res. 81(2), 253-259 (2009).
104. Feinberg AW, Feigel A, Shevkoplyas SS, Sheehy S, Whitesides GM, Parker KK: Muscular thin films for building actuators and powering devices. Science 317(5843), 1366-1370 (2007).
105. Liao I, Liu J, Bursac N, Leong K: Effect of electromechanical stimulation on the maturation of myotubes on aligned electrospun fibers. Cell. Mol. Bioeng. 1(2-3), 133-145 (2008).
106. Naito H, Melnychenko I, Didie M et al..: Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114(Suppl. 1), I72-I78 (2006).
107. Baar K, Birla R, Boluyt MO, Borschel GH, Arruda EM, Dennis RG: Self-organization of rat cardiac cells into contractile 3D cardiac tissue. FASEB J. 19(2), 275-277 (2005).
108. Black LD, Meyers JD, Weinbaum JS, Shvelidze YA, Tranquillo RT: Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng. Part A 15(10), 3099-3108 (2009).
109. Cukierman E, Pankov R, Stevens DR, Yamada KM: Taking cell-matrix adhesions to the third dimension. Science 294(5547), 1708-1712 (2001).
110. Yoshioka J, Prince RN, Huang H et al..: Cardiomyocyte hypertrophy and degradation of connexin43 through spatially restricted autocrine/paracrine heparin-binding EGF. Proc. Natl Acad. Sci. USA 102(30), 10622-10627 (2005).
111. Roberts SF, Stinstra JG, Henriquez CS: Effect of nonuniform interstitial space properties on impulse propagation: a discrete multidomain model. Biophys. J. 95(8), 3724-3737 (2008).
112. Miyata A, Dowell JD, Zipes DP, Rubart M: Rate-dependent [K+](o) accumulation in canine right atria in vivo: electrophysiological consequences. Am. J. Physiol. Heart Circ. Physiol. 283(2), H506-H517 (2002).
113. Vandenburgh H, Solerssi R, Shansky J, Adams J, Henderson S: Mechanical stimulation of organogenic cardiomyocyte growth in vitro. Am. J. Physiol. Cell Physiol. 270(39), C1284-C1292 (1996).
114. Zimmermann W, Schneiderbanger K, Schubert P et al.: Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90, 223-230 (2002).
115. Vandenburgh H, Shansky J, Benesch-Lee F et al.: Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 37(4), 438-447 (2008).
116. Legant WR, Pathak A, Yang MT, Deshpande VS, Mcmeeking RM, Chen CS: Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc. Natl Acad. Sci. USA 106(25), 10097-10102 (2009).