Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium

FASEB Journal

Volumn 28, Issue 2, 2014, Pages 644-654

  Turnbull, Irene C ^a   Karakikes, Ioannis ^a   Serrao, Gregory W ^a   Backeris, Peter ^a   Lee, Jia Jye ^a   Xie, Chaoqin ^a   Senyei, Grant ^a   Gordon, Ronald E ^a   Li, Ronald A ^a,b,c   Akar, Fadi G ^a   Hajjar, Roger J ^a   Hulot, Jean Sébastien ^a,d   Costa, Kevin D ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d Institute OfCardiometabolism and Nutrition   (France)

Author keywords

Cardiomyocyte development; Contractile function; Drug discovery; Stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CALCIUM CHLORIDE; ELASTOMER; GAP JUNCTION PROTEIN; ISOPRENALINE; MESSENGER RNA; MYOSIN HEAVY CHAIN ALPHA; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; VERAPAMIL;

ADULT; ARTICLE; CELL INTERACTION; CHRONOTROPISM; CONTROLLED STUDY; ELECTROSTIMULATION; EMBRYO; EMBRYONIC STEM CELL; GENE TRANSFER; HEART ELECTROPHYSIOLOGY; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE POTENTIAL; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; INOTROPISM; MUSCLE TWITCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; STARLING LAW; TISSUE ENGINEERING; TRANSLATIONAL RESEARCH; CARDIOMYOCYTE DEVELOPMENT; CELL LINE; CONTRACTILE FUNCTION; CYTOLOGY; DRUG DEVELOPMENT; ELECTROPHYSIOLOGY; METHODOLOGY; STEM CELL;

CARDIOMYOCYTE DEVELOPMENT; CONTRACTILE FUNCTION; DRUG DISCOVERY; STEM CELL;

CELL LINE; ELECTROPHYSIOLOGY; HUMANS; MYOCARDIUM; TISSUE ENGINEERING;

EID: 84897066639     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228007     Document Type: Article

References (54)

1. Foldes, G., Mioulane, M., Wright, J. S., Liu, A. Q., Novak, P., Merkely, B., Gorelik, J., Schneider, M. D., Ali, N. N., and Harding, S. E. (2011) Modulation of human embryonic stem cell-derived cardiomyocyte growth: a testbed for studying human cardiac hypertrophy? J. Mol. Cell. Cardiol. 50, 367-376
2. Caspi, O., Lesman, A., Basevitch, Y., Gepstein, A., Arbel, G., Habib, I. H., Gepstein, L., and Levenberg, S. (2007) Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ. Res. 100, 263-272
3. Engler, A. J., Carag-Krieger, C., Johnson, C. P., Raab, M., Tang, H. Y., Speicher, D. W., Sanger, J. W., Sanger, J. M., and Discher, D. E. (2008) Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121, 3794-3802
4. Jacot, J. G., McCulloch, A. D., and Omens, J. H. (2008) Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys. J. 95, 3479-3487
5. Tiburcy, M., Didie, M., Boy, O., Christalla, P., Doker, S., Naito, H., Karikkineth, B. C., El-Armouche, A., Grimm, M., Nose, M., Eschenhagen, T., Zieseniss, A., Katschinksi, D. M., Hamdani, N., Linke, W. A., Yin, X., Mayr, M., and Zimmermann, W. H. (2011) Terminal differentiation, advanced organotypic maturation, and modeling of hypertrophic growth in engineered heart tissue. Circ. Res. 109, 1105-1114
6. Liau, B., Christoforou, N., Leong, K. W., and Bursac, N. (2011) Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function. Biomaterials 32, 9180-9187
7. Song, H., Yoon, C., Kattman, S. J., Dengler, J., Masse, S., Thavaratnam, T., Gewarges, M., Nanthakumar, K., Rubart, M., Keller, G. M., Radisic, M., and Zandstra, P. W. (2010) Interrogating functional integration between injected pluripotent stem cell-derived cells and surrogate cardiac tissue. Proc. Natl. Acad. Sci. U. S. A. 107, 3329-3334
8. Lesman, A., Habib, M., Caspi, O., Gepstein, A., Arbel, G., Levenberg, S., and Gepstein, L. (2010) Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng. A 16, 115-125
9. Zhang, D., Shadrin, I. Y., Lam, J., Xian, H. Q., Snodgrass, H. R., and Bursac, N. (2013) Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34, 5813-5820
10. Stevens, K. R., Pabon, L., Muskheli, V., and Murry, C. E. (2009) Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng. A 15, 1211-1222
11. Stevens, K. R., Kreutziger, K. L., Dupras, S. K., Korte, F. S., Regnier, M., Muskheli, V., Nourse, M. B., Bendixen, K., Reinecke, H., and Murry, C. E. (2009) Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. U. S. A. 106, 16568-16573
12. Nirmalanandhan, V. S., and Sittampalam, G. S. (2009) Stem cells in drug discovery, tissue engineering, and regenerative medicine: emerging opportunities and challenges. J. Biomol. Screen. 14, 755-768
13. Kraehenbuehl, T. P., Langer, R., and Ferreira, L. S. (2011) Three-dimensional biomaterials for the study of human pluripotent stem cells. Nat. Methods 8, 731-736
14. Domian, I. J., Chiravuri, M., van der Meer, P., Feinberg, A. W., Shi, X., Shao, Y., Wu, S. M., Parker, K. K., and Chien, K. R. (2009) Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326, 426-429
15. Boudou, T., Legant, W. R., Mu, A., Borochin, M. A., Thavandiran, N., Radisic, M., Zandstra, P. W., Epstein, J. A., Margulies, K. B., and Chen, C. S. (2012) A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng. A 18, 910-919
16. Tulloch, N. L., Muskheli, V., Razumova, M. V., Korte, F. S., Regnier, M., Hauch, K. D., Pabon, L., Reinecke, H., and Murry, C. E. (2011) Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 109, 47-59
17. Eschenhagen, T., Eder, A., Vollert, I., and Hansen, A. (2012) Physiological aspects of cardiac tissue engineering. Am. J. Physiol. Heart Circ. Physiol. 303, H133-H143
18. Schaaf, S., Shibamiya, A., Mewe, M., Eder, A., Stohr, A., Hirt, M. N., Rau, T., Zimmermann, W. H., Conradi, L., Eschenhagen, T., and Hansen, A. (2011) Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One 6, e26397
19. Kensah, G., Roa Lara, A., Dahlmann, J., Zweigerdt, R., Schwanke, K., Hegermann, J., Skvorc, D., Gawol, A., Azizian, A., Wagner, S., Maier, L. S., Krause, A., Drager, G., Ochs, M., Haverich, A., Gruh, I., and Martin, U. (2013) Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur. Heart J. 34, 1134-1146
20. Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., and Thomson, J. A. (2006) Feeder-independent culture of human embryonic stem cells. Nat. Methods 3, 637-646
21. Karakikes, I., Senyei, G. D., Hansen, J., Kong, C. W., Azeloglu, E. U., Stillitano, F., Lieu, D. K., Wang, J., Ren, L., Hulot, J. S., Iyengar, R., Li, R. A., and Hajjar, R. J. (2013) Small molecule- mediated directed differentiation of human embryonic stem cells toward ventricular cardiomyocytes. Stem Cells Transl. Med. doi: 10.5966/sctm.2013-0110
22. Serrao, G. W., Turnbull, I. C., Ancukiewicz, D., Kim do, E., Kao, E., Cashman, T. J., Hadri, L., Hajjar, R. J., and Costa, K. D. (2012) Myocyte-depleted engineered cardiac tissues support therapeutic potential of mesenchymal stem cells. Tissue Eng. A 18, 1322-1333
23. Akar, F. G., Spragg, D. D., Tunin, R. S., Kass, D. A., and Tomaselli, G. F. (2004) Mechanisms underlying conduction slowing and arrhythmogenesis in nonischemic dilated cardiomyopathy. Circ. Res. 95, 717-725
24. Luo, J., Deng, Z. L., Luo, X., Tang, N., Song, W. X., Chen, J., Sharff, K. A., Luu, H. H., Haydon, R. C., Kinzler, K. W., Vogelstein, B., and He, T. C. (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2, 1236-1247
25. 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, 962-968
26. Naito, H., Melnychenko, I., Didie, M., Schneiderbanger, K., Schubert, P., Rosenkranz, S., Eschenhagen, T., and Zimmermann, W. H. (2006) Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114, I72-78
27. Radisic, M., Park, H., Martens, T. P., Salazar-Lazaro, J. E., Geng, W., Wang, Y., Langer, R., Freed, L. E., and Vunjak-Novakovic, G. (2008) Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J. Biomed. Mater. Res. A. 86, 713-724
28. Chang, M. G., Tung, L., Sekar, R. B., Chang, C. Y., Cysyk, J., Dong, P., Marban, E., and Abraham, M. R. (2006) Proarrhythmic potential of mesenchymal stem cell transplantation revealed in an in vitro coculture model. Circulation 113, 1832-1841
29. Peters, N. S., Severs, N. J., Rothery, S. M., Lincoln, C., Yacoub, M. H., and Green, C. R. (1994) Spatiotemporal relation between gap junctions and fascia adherens junctions during postnatal development of human ventricular myocardium. Circulation 90, 713-725
30. Didie, M., Christalla, P., Rubart, M., Muppala, V., Doker, S., Unsold, B., El-Armouche, A., Rau, T., Eschenhagen, T., Schwoerer, A. P., Ehmke, H., Schumacher, U., Fuchs, S., Lange, C., Becker, A., Tao, W., Scherschel, J. A., Soonpaa, M. H., Yang, T., Lin, Q., Zenke, M., Han, D. W., Scholer, H. R., Rudolph, C., Steinemann, D., Schlegelberger, B., Kattman, S., Witty, A., Keller, G., Field, L. J., and Zimmermann, W. H. (2013) Parthenogenetic stem cells for tissue-engineered heart repair. J. Clin. Invest. 123, 1285-1298
31. Razeghi, P., Young, M. E., Alcorn, J. L., Moravec, C. S., Frazier, O. H., and Taegtmeyer, H. (2001) Metabolic gene expression in fetal and failing human heart. Circulation 104, 2923-2931
32. Hansen, A., Eder, A., Bonstrup, M., Flato, M., Mewe, M., Schaaf, S., Aksehirlioglu, B., Schwoerer, A. P., Uebeler, J., and Eschenhagen, T. (2010) Development of a drug screening platform based on engineered heart tissue. Circ. Res. 107, 35-44
33. Rossman, E. I., Petre, R. E., Chaudhary, K. W., Piacentino, V., 3rd, Janssen, P. M., Gaughan, J. P., Houser, S. R., and Margulies, K. B. (2004) Abnormal frequency-dependent responses represent the pathophysiologic signature of contractile failure in human myocardium. J. Mol. Cell. Cardiol. 36, 33-42
34. Wiegerinck, R. F., Cojoc, A., Zeidenweber, C. M., Ding, G., Shen, M., Joyner, R. W., Fernandez, J. D., Kanter, K. R., Kirshbom, P. M., Kogon, B. E., and Wagner, M. B. (2009) Force frequency relationship of the human ventricle increases during early postnatal development. Pediatr. Res. 65, 414-419
35. Holubarsch, C., Ruf, T., Goldstein, D. J., Ashton, R. C., Nickl, W., Pieske, B., Pioch, K., Ludemann, J., Wiesner, S., Hasenfuss, G., Posival, H., Just, H., and Burkhoff, D. (1996) Existence of the Frank-Starling mechanism in the failing human heart. Investigations on the organ, tissue, and sarcomere levels. Circulation 94, 683-689
36. Schwinger, R. H., Bohm, M., and Erdmann, E. (1992) Inotropic and lusitropic dysfunction in myocardium from patients with dilated cardiomyopathy. Am. Heart. J. 123, 116-128
37. Pillekamp, F., Haustein, M., Khalil, M., Emmelheinz, M., Nazzal, R., Adelmann, R., Nguemo, F., Rubenchyk, O., Pfannkuche, K., Matzkies, M., Reppel, M., Bloch, W., Brockmeier, K., and Hescheler, J. (2012) Contractile properties of early human embryonic stem cell-derived cardiomyocytes: adrenergic stimulation induces positive chronotropy and lusitropy but not inotropy. Stem Cells Dev. 21, 2111-2121
38. Gwathmey, J. K., Warren, S. E., Briggs, G. M., Copelas, L., Feldman, M. D., Phillips, P. J., Callahan, M., Jr., Schoen, F. J., Grossman, W., and Morgan, J. P. (1991) Diastolic dysfunction in hypertrophic cardiomyopathy. Effect on active force generation during systole. J. Clin. Invest. 87, 1023-1031
39. Cooper, I. C., and Fry, C. H. (1990) Mechanical restitution in isolated mammalian myocardium: species differences and underlying mechanisms. J. Mol. Cell. Cardiol. 22, 439-452
40. Schwinger, R. H., Bohm, M., and Erdmann, E. (1990) Negative inotropic properties of isradipine, nifedipine, diltiazem, and verapamil in diseased human myocardial tissue. J. Cardiovasc. Pharmacol. 15, 892-899
41. Hasenfuss, G., Mulieri, L. A., Leavitt, B. J., and Alpert, N. R. (1994) Influence of isoproterenol on contractile protein function, excitation- contraction coupling, and energy turnover of isolated nonfailing human myocardium. J. Mol. Cell. Cardiol. 26, 1461-1469
42. Hasenfuss, G., Mulieri, L. A., Allen, P. D., Just, H., and Alpert, N. R. (1996) Influence of isoproterenol and ouabain on excitationcontraction coupling, cross-bridge function, and energetics in failing human myocardium. Circulation 94, 3155-3160
43. Sonnenblick, E. H., Ross, J., Jr., Covell, J. W., and Braunwald, E. (1966) Alterations in resting length-tension relations of cardiac muscle induced by changes in contractile force. Circ. Res. 19, 980-988
44. Cain, B. S., Meldrum, D. R., Meng, X., Shames, B. D., Banerjee, A., and Harken, A. H. (1998) Calcium preconditioning in human myocardium. Ann. Thorac. Surg. 65, 1065-1070
45. Godt, R. E., Fogaca, R. T., and Nosek, T. M. (1991) Changes in force and calcium sensitivity in the developing avian heart. Can. J. Physiol. Pharmacol. 69, 1692-1697
46. Bohm, M., Morano, I., Pieske, B., Ruegg, J. C., Wankerl, M., Zimmermann, R., and Erdmann, E. (1991) Contribution of cAMPphosphodiesterase inhibition and sensitization of the contractile proteins for calcium to the inotropic effect of pimobendan in the failing human myocardium. Circ. Res. 68, 689-701
47. White, M., Roden, R., Minobe, W., Khan, M. F., Larrabee, P., Wollmering, M., Port, J. D., Anderson, F., Campbell, D., Feldman, A. M. (1994) Age-related changes in -adrenergic neuroeffector systems in the human heart. Circulation 90, 1225-1238
48. Franz, M. R., Swerdlow, C. D., Liem, L. B., and Schaefer, J. (1988) Cycle length dependence of human action potential duration in vivo. Effects of single extrastimuli, sudden sustained rate acceleration and deceleration, and different steadystate frequencies. J. Clin. Invest. 82, 972-979
49. Xu, C., Police, S., Rao, N., and Carpenter, M. K. (2002) Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res. 91, 501-508
50. Liu, J., Lieu, D. K., Siu, C. W., Fu, J. D., Tse, H. F., and Li, R. A. (2009) Facilitated maturation of Ca2+ handling properties of human embryonic stem cell-derived cardiomyocytes by calsequestrin expression. Am. J. Physiol. Cell Physiol. 297, C152-C159
51. Fulbright, J. M. (2011) Review of cardiotoxicity in pediatric cancer patients: during and after therapy. Cardiol. Res. Pract. 2011, 942090
52. Carlsson, L. (2006) In vitro and in vivo models for testing arrhythmogenesis in drugs. J. Intern. Med. 259, 70-80
53. Liang, H., Matzkies, M., Schunkert, H., Tang, M., Bonnemeier, H., Hescheler, J., and Reppel, M. (2010) Human and murine embryonic stem cell-derived cardiomyocytes serve together as a valuable model for drug safety screening. Cell. Physiol. Biochem. 25, 459-466
54. Peng, S., Lacerda, A. E., Kirsch, G. E., Brown, A. M., and Bruening-Wright, A. (2010) The action potential and comparative pharmacology of stem cell-derived human cardiomyocytes. J. Pharmacol. Toxicol. Methods 61, 277-286