Myocardial tissue engineering: In vitro models

Cold Spring Harbor Perspectives in Medicine

Volumn 4, Issue 3, 2014, Pages

  Vunjak Novakovic, Gordana ^a   Eschenhagen, Thomas ^b,c   Mummery, Christine ^d  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ATORVASTATIN; BIOMATERIAL; BONE MORPHOGENETIC PROTEIN; COLLAGEN; DESMIN; DOFETILIDE; ERYTHROMYCIN; FIBRIN; FIBROBLAST GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HYALURONIC ACID; MATRIGEL; MESSENGER RNA; MYOCYTE ENHANCER FACTOR 2; MYOSIN; POLYCOMB REPRESSIVE COMPLEX 2; POLYGLACTIN; POLYLACTIC ACID; POLYURETHAN; POTASSIUM CHANNEL HERG; PROTEIN KINASE C ALPHA; QUINIDINE; SCLEROPROTEIN; THIORIDAZINE; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX5; TRASTUZUMAB; TROPONIN; UNINDEXED DRUG;

APOPTOSIS; ARTICLE; CARDIOTOXICITY; CELL FUNCTION; CELL MATURATION; DISEASE COURSE; DRUG SCREENING; ENDOTHELIUM CELL; GENE EXPRESSION; HEART FAILURE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HIGH THROUGHPUT SCREENING; HUMAN; IMPLANTATION; IN VITRO STUDY; MUSCLE DEVELOPMENT; NEOPLASM; NONHUMAN; PHYSIOLOGY; PLURIPOTENT STEM CELL; STEM CELL; TISSUE ENGINEERING; TISSUE REGENERATION;

BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; HUMANS; MODELS, BIOLOGICAL; MYOCARDIUM; MYOCYTES, CARDIAC; TISSUE ENGINEERING; TOXICITY TESTS;

EID: 84897595636     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a014076     Document Type: Article

References (80)

1. Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. 2006.Tissueengineered autologous bladders for patients needing cystoplasty. The Lancet 367: 1241-1246.
2. Birla RK, Borschel GH, Dennis RG, Brown DL. 2005. Myocardial engineering in vivo: Formation and characterization of contractile, vascularized three-dimensional cardiac tissue. Tissue Eng 11: 803-813.
3. Boudou T, Legant WR, Mu A, Borochin MA, Thavandiran N, Radisic M, Zandstra PW, Epstein JA, Margulies KB, Chen CS. 2012 A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng Part A 18: 910-919.
4. Buckingham M, Meilhac S, Zaffran S. 2005. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6: 826-835.
5. Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R, Vunjak-Novakovic G, Freed LE. 1999. Cardiac muscle tissue engineering: Towards an in vitro model for electrophysiological studies. Am J Physiol 277: H433-H444.
6. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5: 877-889.
7. Carrier R, Papadaki M, Rupnick M, Schoen FJ, Bursac N, Langer R, Freed LE, Vunjak-Novakovic G. 1999. Cardiac tissue engineering: Cell seeding, cultivation parameters and tissue construct characterization. Biotechnol Bioeng 64: 580-589.
8. Caspi O, Lesman A, Basevitch Y, Gepstein A, Arbel G, Habib IH, Gepstein L, Levenberg S. 2007. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100: 263-272.
9. Christman KL, Vardanian AJ, Fang Q, Sievers RE, Fok HH, Lee RJ. 2004. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol 44: 654-660.
10. Chung CS, Granzier HL. 2011. Contribution of titin and extracellular matrix to passive pressure and measurement of sarcomere length in the mouse left ventricle. JMol Cell Cardiol 50: 731-739.
11. Dahl SLM, Kypson AP, Lawson JH, Blum JL, Strader JT, Li Y, Manson RJ, Tente WE, DiBernardo L, Hensley MT, et al. 2011. Readily available tissue-engineered vascular grafts. Sci Transl Med 3: 68-79.
12. Darpo B, Nebout T, Sager PT. 2006. Clinical evaluation of QT/QTc interval prolongation and proarrhythmic potential for non-antiarrhythmic drugs. J Clin Pharmacol 46: 498-507.
13. Davis RP, van den Berg CW, Casini S, Braam SR, Mummery CL. 2011. Pluripotent stem cell models of cardiac disease and their implication for drug discovery and development. Trends Mol Med 17: 475-484.
14. Davis RP, Casini S, van den Berg CW, Hoekstra M, Remme CA, Dambrot C, Salvatori D, Oostwaard DW, Wilde AA, Bezzina CR, et al. 2012. Cardiomyocytes derived from pluripotent stem cells recapitulate electrophysiological characteristics of an overlap syndrome of cardiac sodium channel disease. Circulation 125: 3079-3091.
15. de Lange WJ, Hegge LF, Grimes AC, Tong CW, Brost TM, Moss RL, Ralphe JC. 2011. Neonatal mouse-derived engineered cardiac tissue: A novel model system for studying genetic heart disease. Circ Res 109: 8-19.
16. Duan Y, Liu Z, O'Neill J, Wan L, Freytes DO, Vunjak-Novakovic G. 2011.Hydrogel derived from native heart matrix induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. J Cardiovasc Transl Research 4: 605-615.
17. El-Armouche A, Singh J, Naito H, Wittköpper K, Didié M, Laatsch A, Zimmermann WH, Eschenhagen T. 2007. Adenovirus-delivered short hairpin RNA targeting PKC-a improves contractile function in reconstituted heart tissue. J Mol Cell Cardiol 43: 371-376.
18. Elliott DA, Braam SR, Koutsis K, Ng ES, Jenny R, Lagerqvist EL, Biben C, Hatzistavrou T, Hirst CE, Yu QC, et al. 2011. NKX2-5eGFP/w hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods 8: 1037-1040.
19. Engelmayr GC Jr, Cheng M, Bettinger CJ, Borenstein JT, Langer R, Freed LE. 2008. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 7: 1003-1010.
20. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006 Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
21. Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J, Zimmermann W, Dohmen HH, Schäfer H, Bishopric N, et al. 1997. Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: A new heart muscle model system. FASEB J 11: 683-694.
22. Eschenhagen T, Didié M, Heubach J, Ravens U, Zimmermann WH. 2002. Cardiac tissue engineering. Transpl Immunol 9: 315-321.
23. Eschenhagen T, Force T, Ewer MS, de Keulenaar GW, Suter TM, Anker SD, Avkiran M, de Azambuja W, Balligand JL, Brutsaert DL, et al. 2011. Cardiovascular side effects of cancer therapies: A position statement from the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 13: 1-10.
24. Eschenhagen T, Eder A, Vollert I, Hansen A. 2012. Physiological aspects of cardiac tissue engineering. Am J Physiol Heart Circ Physiol 303: H133-H143.
25. Fenichel RR, Malik M, Antzelevitch C, Sanguinetti M, Roden DM, Priori SG, Ruskin JN, Lipicky RJ, Cantilena LR. 2004. Drug-induced torsades de pointes and implications for drug development. J Cardiovasc Electrophysiol 15: 475-495.
26. Fomovsky GM, Thomopoulos S, Holmes JW. 2010. Contribution of extracellular matrix to the mechanical properties of the heart. J Mol Cell Cardiol 48: 490-496.
27. Force T. 2012. Double-edged sword of the new cancer therapeutics. Circulation 125: 2057-2058.
28. Force T, Kolaja KL. 2011. Cardiotoxicity of kinase inhibitors: The prediction and translation of preclinical models to clinical outcomes. Nat Rev Drug Discov 10: 111-126.
29. Friedrich FW, Wilding BR, Reischmann S, Crocini C, Lang P, Charron P, Müller OJ, McGrath MJ, Vollert I, Hansen A, et al. 2012. Evidence for FHL1 as a novel disease gene for isolated hypertrophic cardiomyopathy. Hum Mol Genet 21: 3237-3254.
30. Godier-Furnémont A, Martens T, Koeckert M, Wan LQ, Parks J, Zhang G, Hudson J, Vunjak-Novakovic G. 2011. Composite scaffold provides a cell delivery platform for cardiovascular repair. Proc Natl Acad Sci 108: 7974-7979 [Research highlights. 2011. Bioengineering Bio: Patching up the heart. Nature 472: 393
31. Godier-Furnémont AFG, Vunjak-Novakovic G. 2012. Cardiac muscle tissue engineering. In Biomaterials science: An introduction to materials in medicine, 3rd ed. (ed. Ratner B, Hofman A, Lemons JE, Schoen FJ). Academic, San Diego.
32. Goumans MJ, de Boer TP, Smits AM, van Laake LW, van Vliet P, Metz CH, Korfage TH, Kats KP, Hochstenbach R, Pasterkamp G, et al. 2007. TGF-b1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 1: 138-149.
33. Hansen A, Eder A, Bönstrup M, Flato M, Mewe M, Schaaf S, Aksehirlioglu B, Schwoerer AP, Uebeler J, Eschenhagen T. 2010. Development of a drug screening platform based on engineered heart tissue. Circ Res 107: 35-44.
34. He A, Ma Q, Cao J, von Gise A, Zhou P, Xie H, Zhang B, Hsing M, Christodoulou D, Cahan P, et al. 2012. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ Res 110: 406-415.
35. Hirt MN, Sörensen NA, Bartholdt LM, Boeddinghaus J, Schaaf S, Eder A, Vollert I, Stöhr A, Schulze T, Witten A, et al. 2012. Increased afterload induces pathological cardiac hypertrophy: A new in vitro model. Basic Res Cardiol 107: 307.
36. Hirt M, Hansen A, Eschenhagen T. 2014. Cardiac tissue engineering-State of the art. Circ Res 114: 354-367.
37. Ishii O, Shin M, Sueda T, Vacanti JP. 2005. In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix-like topography. J Thorac Cardiovasc Surg 130: 1358-1363.
38. Kattman SJ, Witty AD, Gagliardi M, Dubois NC, Niapour M, Hotta A, Ellis J, Keller G. 2011. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8: 228-240.
39. Khademhosseini A, Eng G, Yeh J, Kucharczyk P, Langer R, Vunjak-Novakovic G, Radisic M. 2007. Microfluidic patterning for fabrication of contractile cardiac organoids. Biomed Microdevices 9: 149-157.
40. Laflamme M, Chen K, Naumova A, Muskheli V, Fugate J, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, et al. 2007. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024.
41. Langer R, Tirrell DA. 2004. Designing materials for biology and medicine. Nature 428: 487-492.
42. Lieu DK, Liu J, Siu CW, McNerney GP, Tse HF, Abu-Khalil A, Huser T, Li RA. 2009. Absence of transverse tubules contributes to non-uniform Ca2{thorn} wavefronts in mouse and human embryonic stem cell-derived cardiomyocytes. Stem Cells Dev 18: 1493-1500.
43. Lutolf MP, Hubbell JA. 2005. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23: 47-55.
44. Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Dodson A, Martorell J, Bellini S, Parnigotto PP, et al. 2008. Clinical transplantation of a tissue-engineered airway. Lancet 372: 2023-2030.
45. Majesky MW, Mummery CL. 2012. Smooth muscle diversity from human pluripotent cells. Nat Biotechnol 30: 152-154.
46. Marsano A, Maidhof R, Wan LQ, Wang Y, Gao J, Tandon N, Vunjak-Novakovic G. 2010. Scaffold stiffness affects the contractile function of engineered cardiac constructs. Biotechnol Prog 26: 1382-1390.
47. Marsano A, Maidhof R, Luo J, Fujikara K, Konofagou E, Banfi A, Vunjak-Novakovic G. 2013. Controlled expression of VEGF by transduced cells in a cardiac patch improves vascularization and cardiac function in a mouse model of myocardial infarction. Biomaterials 34: 393-401.
48. McDevitt TC, Laflamme MA, Murry CE. 2005. Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI3-kinase/Akt signaling pathway. J Mol Cell Cardiol 39: 865-873.
49. Meilhac SM, Esner M, Kelly RG, Nicolas JF, Buckingham ME. 2004. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell 6: 685-698.
50. Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R, Norris RA, Kern MJ, Eisenberg CA, Turner D, Markwald RR. 2001. The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol 238: 97-109.
51. Mühlhäuser U, Zolk O, Rau T, Münzel F, Wieland T, Eschenhagen T. 2006. Atorvastatin desensitizes b-adrenergic signaling in cardiac myocytes via reduced isoprenylation of G-protein g-subunits. FASEB J 20: 785-787.
52. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, et al. 2003. Differentiation of human embryonic stem cells to cardiomyocytes: Role of coculture with visceral endodermlike cells. Circulation 107: 2733-2740.
53. Mummery CL, Zhang J, Ng ES, Elliott DA, Elefanty AG, Kamp TJ. 2012. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: A methods overview. Circ Res 111: 344-358.
54. Olson EN, Schneider MD. 2003. Sizing up the heart: Development redux in disease. Genes Dev 17: 1937-1956.
55. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. 2008. Perfusion-decellularized matrix:Using nature's platform to engineer a bioartificial heart. Nat Med 14: 213-221.
56. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I, Gianni L, Baselga J, Bell R, Jackisch C, et al. 2011. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 353: 1659-1672.
57. Radisic M, Park H, Shing H, Consi T, Schoen F, Langer R, Freed LE, Vunjak-Novakovic G. 2004a. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci 101: 18129-18134.
58. Radisic M, Yang L, Boublik J, Cohen RJ, Langer R, Freed LE, Vunjak-Novakovic G. 2004b. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol 286: H507-H516.
59. Radisic M, Park H, Chen F, Wang Y, Dennis R, Langer R, Freed LE, Vunjak-Novakovic G. 2006. Biomimetic approach to cardiac tissue engineering: Oxygen carriers and channeled scaffolds. Tissue Eng 12: 2077-2091.
60. Robinson KA, Li J, Mathison M, Redkar A, Cui J, Chronos NA, Matheny RG, Badylak SF. 2005. Extracellular matrix scaffold for cardiac repair. Circulation 112: I135-I143.
61. Schaaf S, Shibamiya A, Mewe M, Eder A, Stöhr A, Hirt MN, Rau T, Zimmermann WH, Conradi L, Eschenhagen T, et al. 2011.Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS ONE 6: e26397.
62. Sheehy SP, Grosberg A, Paker KK. 2012. The contribution of cellular mechanostransduction to cardiomyocyte form and function. Biomech Model Mechanobiol 11: 1223-1227.
63. Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K, Kikuchi A, Umezu M, Okano T. 2002. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90: e40.
64. Singelyn JM, Sundaramurthy S, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM, Wang J, Mayle KM, Bartels K, Salvatore M, et al. 2012. Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. JACC 59: 751-763.
65. Smits AM, van Vliet P, Metz CH, Korfage T, Sluijter JP, Doevendans PA, Goumans MJ. 2009. Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: An in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc 4: 232-243.
66. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
67. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
68. Tibbitt MW, Anseth KS. 2009. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 103: 655-663.
69. Tiburcy M, Didie M, Boy O, Christalla P, Doker S, Naito H, Karikkineth BC, El-Armouche A, Grimm M, Nose M, et al. 2011. Terminal differentiation, advanced organotypic maturation, and modeling of hypertrophic growth in engineered heart tissue. Circ Res 109: 1105-1114.
70. Vunjak-Novakovic G, Scadden DT. 2011. Biomimetic platforms for human stem cell research. Cell Stem Cell 8: 252-261.
71. Vunjak-Novakovic G, Tandon N, Godier A, Martens T, Maidhof R, Marsano A, Radisic M. 2010. Challenges in cardiac tissue engineering. Tissue Eng Part B Rev 16: 169-187.
72. Vunjak-Novakovic G, Lui KO, Tandon N, Chien K. 2011. Bioengineering heart muscle: A paradigm for regenerative medicine. Annual Rev Biomed Eng 13: 245-267.
73. Waldo KL, Kumiski DH, Wallis KT, Stadt HA, Hutson MR, Platt DH, Kirby ML. 2001. Conotruncal myocardium arises from a secondary heart field. Development 128: 3179-3188.
74. Wobus AM, Boheler KR. 2005. Embryonic stem cells: Prospects for developmental biology and cell therapy. Physiol Rev 85: 635-678.
75. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, et al. 2008. Human cardiovascular progenitor cells develop from a KDR{thorn} embryonic-stem-cell-derived population. Nature 453: 524-528.
76. You Z, Cao H, Gao J, Shin PH, Day BW, Wang Y. 2010. A functionalizable polyester with free hydroxyl groups and tunable physiochemical and biological properties. Biomaterials 31: 3129-3138.
77. Zimmermann WH, Fink C, Kralisch D, Remmers U, Weil J, Eschenhagen T. 2000. Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68: 106-114.
78. Zimmermann WH, Schneiderbanger K, Schubert P, Didié M, Münzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T. 2002. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90: 223-230.
79. Zimmermann WH, Melnychenko I, Eschenhagen T. 2004. Engineered heart tissue for regeneration of diseased hearts. Biomaterials 25: 1639-1647.
80. Zimmermann W, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, et al. 2006. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12: 452-458.