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Published in: Pediatric Cardiology 5/2009

Open Access 01-07-2009 | Riley Symposium

Cardiac Tissue Engineering: Implications for Pediatric Heart Surgery

Authors: Wolfram-Hubertus Zimmermann, Robert Cesnjevar

Published in: Pediatric Cardiology | Issue 5/2009

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Abstract

Children with severe congenital malformations, such as single-ventricle anomalies, have a daunting prognosis. Heart transplantation would be a therapeutic option but is restricted due to a lack of suitable donor organs and, even in case of successful heart transplantation, lifelong immune suppression would frequently be associated with a number of serious side effects. As an alternative to heart transplantation and classical cardiac reconstructive surgery, tissue-engineered myocardium might become available to augment hypomorphic hearts and/or provide new muscle material for complex myocardial reconstruction. These potential applications of tissue engineered myocardium will, however, impose major challenges to cardiac tissue engineers as well as heart surgeons. This review will provide an overview of available cardiac tissue-engineering technologies, discuss limitations, and speculate on a potential application of tissue-engineered heart muscle in pediatric heart surgery.
Literature
1.
go back to reference Akins RE, Boyce RA, Madonna ML, Schroedl NA, Gonda SR, McLaughlin TA, Hartzell CR (1999) Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. Tissue Eng 5:103–118PubMedCrossRef Akins RE, Boyce RA, Madonna ML, Schroedl NA, Gonda SR, McLaughlin TA, Hartzell CR (1999) Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. Tissue Eng 5:103–118PubMedCrossRef
2.
go back to reference Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S (2003) Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 107:1024–1032PubMedCrossRef Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S (2003) Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 107:1024–1032PubMedCrossRef
3.
go back to reference Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668–673PubMedCrossRef Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668–673PubMedCrossRef
4.
go back to reference Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R, Vunjak-Novakovic G, Freed LE (1999) Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol 277:H433–H444PubMed Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R, Vunjak-Novakovic G, Freed LE (1999) Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol 277:H433–H444PubMed
5.
go back to reference Carrier RL, 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 64:580–589PubMedCrossRef Carrier RL, 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 64:580–589PubMedCrossRef
6.
go back to reference 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 100:263–272PubMedCrossRef 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 100:263–272PubMedCrossRef
7.
go back to reference Chachques JC, Trainini JC, Lago N, Cortes-Morichetti M, Schussler O, Carpentier A (2008) Myocardial Assistance by Grafting a New Bioartificial Upgraded Myocardium (MAGNUM trial): clinical feasibility study. Ann Thorac Surg 85:901–908PubMedCrossRef Chachques JC, Trainini JC, Lago N, Cortes-Morichetti M, Schussler O, Carpentier A (2008) Myocardial Assistance by Grafting a New Bioartificial Upgraded Myocardium (MAGNUM trial): clinical feasibility study. Ann Thorac Surg 85:901–908PubMedCrossRef
8.
go back to reference Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87:27–45PubMed Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87:27–45PubMed
9.
go back to reference 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 7:1003–1010PubMedCrossRef 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 7:1003–1010PubMedCrossRef
10.
go back to reference Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J, Zimmermann W, Dohmen HH, Schafer H, Bishopric N, Wakatsuki T, Elson EL (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11:683–694PubMed Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J, Zimmermann W, Dohmen HH, Schafer H, Bishopric N, Wakatsuki T, Elson EL (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11:683–694PubMed
11.
12.
go back to reference Fink Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14:669–679 Fink Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14:669–679
13.
go back to reference Furuta A, Miyoshi S, Itabashi Y, Shimizu T, Kira S, Hayakawa K, Nishiyama N, Tanimoto K, Hagiwara Y, Satoh T, Fukuda K, Okano T, Ogawa S (2006) Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res 98:705–712PubMedCrossRef Furuta A, Miyoshi S, Itabashi Y, Shimizu T, Kira S, Hayakawa K, Nishiyama N, Tanimoto K, Hagiwara Y, Satoh T, Fukuda K, Okano T, Ogawa S (2006) Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res 98:705–712PubMedCrossRef
14.
go back to reference Gardiner HM (2008) In utero intervention for severe congenital heart disease. Best Pract Res Clin Obstet Gynaecol 22:49–61PubMedCrossRef Gardiner HM (2008) In utero intervention for severe congenital heart disease. Best Pract Res Clin Obstet Gynaecol 22:49–61PubMedCrossRef
15.
16.
go back to reference Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W, Hasenfuss G (2006) Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440:1199–1203PubMedCrossRef Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W, Hasenfuss G (2006) Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440:1199–1203PubMedCrossRef
17.
go back to reference Guo XM, Zhao YS, Chang HX, Wang CY, Ling-Ling E, Zhang XA, Duan CM, Dong LZ, Jiang H, Li J, Song Y, Yang XJ (2006) Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation 113:2229–2237PubMedCrossRef Guo XM, Zhao YS, Chang HX, Wang CY, Ling-Ling E, Zhang XA, Duan CM, Dong LZ, Jiang H, Li J, Song Y, Yang XJ (2006) Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation 113:2229–2237PubMedCrossRef
18.
go back to reference Haraguchi Y, Shimizu T, Yamato M, Kikuchi A, Okano T (2006) Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27:4765–4774PubMedCrossRef Haraguchi Y, Shimizu T, Yamato M, Kikuchi A, Okano T (2006) Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27:4765–4774PubMedCrossRef
19.
go back to reference Huang YC, Khait L, Birla RK (2007) Contractile three-dimensional bioengineered heart muscle for myocardial regeneration. J Biomed Mater Res A 80:719–731PubMed Huang YC, Khait L, Birla RK (2007) Contractile three-dimensional bioengineered heart muscle for myocardial regeneration. J Biomed Mater Res A 80:719–731PubMed
20.
go back to reference Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108:407–414PubMed Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108:407–414PubMed
21.
go back to reference Kelm JM, Ehler E, Nielsen LK, Schlatter S, Perriard JC, Fussenegger M (2004) Design of artificial myocardial microtissues. Tissue Eng 10:201–214PubMedCrossRef Kelm JM, Ehler E, Nielsen LK, Schlatter S, Perriard JC, Fussenegger M (2004) Design of artificial myocardial microtissues. Tissue Eng 10:201–214PubMedCrossRef
22.
go back to reference Kelm JM, Djonov V, Ittner LM, Fluri D, Born W, Hoerstrup SP, Fussenegger M (2006) Design of custom-shaped vascularized tissues using microtissue spheroids as minimal building units. Tissue Eng 12:2151–2160PubMedCrossRef Kelm JM, Djonov V, Ittner LM, Fluri D, Born W, Hoerstrup SP, Fussenegger M (2006) Design of custom-shaped vascularized tissues using microtissue spheroids as minimal building units. Tissue Eng 12:2151–2160PubMedCrossRef
23.
go back to reference Klug MG, Soonpaa MH, Koh GY, Field LJ (1996) Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest 98:216–224PubMedCrossRef Klug MG, Soonpaa MH, Koh GY, Field LJ (1996) Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest 98:216–224PubMedCrossRef
24.
go back to reference Kofidis T, Lenz A, Boublik J, Akhyari P, Wachsmann B, Mueller-Stahl K, Hofmann M, Haverich A (2003) Pulsatile perfusion and cardiomyocyte viability in a solid three-dimensional matrix. Biomaterials 24:5009–5014PubMedCrossRef Kofidis T, Lenz A, Boublik J, Akhyari P, Wachsmann B, Mueller-Stahl K, Hofmann M, Haverich A (2003) Pulsatile perfusion and cardiomyocyte viability in a solid three-dimensional matrix. Biomaterials 24:5009–5014PubMedCrossRef
25.
go back to reference Kofidis T, deBruin JL, Tanaka M, Zwierzchoniewska M, Weissman I, Fedoseyeva E, Haverich A, Robbins RC (2005) They are not stealthy in the heart: embryonic stem cells trigger cell infiltration, humoral and T-lymphocyte-based host immune response. Eur J Cardiothorac Surg 28:461–466PubMedCrossRef Kofidis T, deBruin JL, Tanaka M, Zwierzchoniewska M, Weissman I, Fedoseyeva E, Haverich A, Robbins RC (2005) They are not stealthy in the heart: embryonic stem cells trigger cell infiltration, humoral and T-lymphocyte-based host immune response. Eur J Cardiothorac Surg 28:461–466PubMedCrossRef
26.
go back to reference Kolossov E, Bostani T, Roell W, Breitbach M, Pillekamp F, Nygren JM, Sasse P, Rubenchik O, Fries JW, Wenzel D, Geisen C, Xia Y, Lu Z, Duan Y, Kettenhofen R, Jovinge S, Bloch W, Bohlen H, Welz A, Hescheler J, Jacobsen SE, Fleischmann BK (2006) Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. J Exp Med 203:2315–2327PubMedCrossRef Kolossov E, Bostani T, Roell W, Breitbach M, Pillekamp F, Nygren JM, Sasse P, Rubenchik O, Fries JW, Wenzel D, Geisen C, Xia Y, Lu Z, Duan Y, Kettenhofen R, Jovinge S, Bloch W, Bohlen H, Welz A, Hescheler J, Jacobsen SE, Fleischmann BK (2006) Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. J Exp Med 203:2315–2327PubMedCrossRef
27.
go back to reference Leor J, Aboulafia-Etzion S, Dar A, Shapiro L, Barbash IM, Battler A, Granot Y, Cohen S (2000) Bioengineered cardiac grafts a new approach to repair the infarcted myocardium? Circulation 102:III56–IIII61PubMed Leor J, Aboulafia-Etzion S, Dar A, Shapiro L, Barbash IM, Battler A, Granot Y, Cohen S (2000) Bioengineered cardiac grafts a new approach to repair the infarcted myocardium? Circulation 102:III56–IIII61PubMed
28.
go back to reference Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D’Amore PA, Langer R (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884PubMedCrossRef Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D’Amore PA, Langer R (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884PubMedCrossRef
29.
go back to reference Li RK, Jia ZQ, Weisel RD, Mickle DA, Choi A, Yau TM (1999) Survival and function of bioengineered cardiac grafts. Circulation 100:II63–II69PubMed Li RK, Jia ZQ, Weisel RD, Mickle DA, Choi A, Yau TM (1999) Survival and function of bioengineered cardiac grafts. Circulation 100:II63–II69PubMed
30.
go back to reference Li RK, Yau TM, Weisel RD, Mickle DA, Sakai T, Choi A, Jia ZQ (2000) Construction of a bioengineered cardiac graft. J Thorac Cardiovasc Surg 119:368–375PubMedCrossRef Li RK, Yau TM, Weisel RD, Mickle DA, Sakai T, Choi A, Jia ZQ (2000) Construction of a bioengineered cardiac graft. J Thorac Cardiovasc Surg 119:368–375PubMedCrossRef
31.
go back to reference Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12:459–465PubMedCrossRef Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12:459–465PubMedCrossRef
32.
go back to reference Moorman A, Webb S, Brown NA, Lamers W, Anderson RH (2003) Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 89:806–814PubMedCrossRef Moorman A, Webb S, Brown NA, Lamers W, Anderson RH (2003) Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 89:806–814PubMedCrossRef
33.
go back to reference Morritt AN, Bortolotto SK, Dilley RJ, Han X, Kompa AR, McCombe D, Wright CE, Itescu S, Angus JA, Morrison WA (2007) Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 115:353–360PubMedCrossRef Morritt AN, Bortolotto SK, Dilley RJ, Han X, Kompa AR, McCombe D, Wright CE, Itescu S, Angus JA, Morrison WA (2007) Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 115:353–360PubMedCrossRef
35.
go back to reference Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428:664–668PubMedCrossRef Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428:664–668PubMedCrossRef
36.
go back to reference Naito H, Melnychenko I, Didie M, Schneiderbanger K, Schubert P, Rosenkranz S, Eschenhagen T, Zimmermann WH (2006) Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114:I72–I78PubMedCrossRef Naito H, Melnychenko I, Didie M, Schneiderbanger K, Schubert P, Rosenkranz S, Eschenhagen T, Zimmermann WH (2006) Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114:I72–I78PubMedCrossRef
37.
go back to reference Nygren JM, Jovinge S, Breitbach M, Sawen P, Roll W, Hescheler J, Taneera J, Fleischmann BK, Jacobsen SE (2004) Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10:494–501PubMedCrossRef Nygren JM, Jovinge S, Breitbach M, Sawen P, Roll W, Hescheler J, Taneera J, Fleischmann BK, Jacobsen SE (2004) Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10:494–501PubMedCrossRef
38.
go back to reference Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y (1995) Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials 16:297–303PubMedCrossRef Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y (1995) Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials 16:297–303PubMedCrossRef
39.
go back to reference 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 14:213–221PubMedCrossRef 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 14:213–221PubMedCrossRef
40.
go back to reference Pavlovic M, Acharya G, Huhta JC (2008) Controversies of fetal cardiac intervention. Early Hum Dev 84:149–153PubMedCrossRef Pavlovic M, Acharya G, Huhta JC (2008) Controversies of fetal cardiac intervention. Early Hum Dev 84:149–153PubMedCrossRef
41.
go back to reference Phoon CK, Ji RP, Aristizabal O, Worrad DM, Zhou B, Baldwin HS, Turnbull DH (2004) Embryonic heart failure in NFATc1−/− mice: novel mechanistic insights from in utero ultrasound biomicroscopy. Circ Res 95:92–99PubMedCrossRef Phoon CK, Ji RP, Aristizabal O, Worrad DM, Zhou B, Baldwin HS, Turnbull DH (2004) Embryonic heart failure in NFATc1−/− mice: novel mechanistic insights from in utero ultrasound biomicroscopy. Circ Res 95:92–99PubMedCrossRef
42.
go back to reference Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G (2004) Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 101:18129–18134PubMedCrossRef Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G (2004) Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 101:18129–18134PubMedCrossRef
43.
go back to reference Reinecke H, Zhang M, Bartosek T, Murry CE (1999) Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 100:193–202PubMed Reinecke H, Zhang M, Bartosek T, Murry CE (1999) Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 100:193–202PubMed
44.
go back to reference Rubart M, Pasumarthi KB, Nakajima H, Soonpaa MH, Nakajima HO, Field LJ (2003) Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 92:1217–1224PubMedCrossRef Rubart M, Pasumarthi KB, Nakajima H, Soonpaa MH, Nakajima HO, Field LJ (2003) Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 92:1217–1224PubMedCrossRef
45.
go back to reference Shapira-Schweitzer K, Habib M, Gepstein L, Seliktar D (2009) A photopolymerizable hydrogel for 3-D culture of human embryonic stem cell-derived cardiomyocytes and rat neonatal cardiac cells. J Mol Cell Cardiol 46:213–224PubMedCrossRef Shapira-Schweitzer K, Habib M, Gepstein L, Seliktar D (2009) A photopolymerizable hydrogel for 3-D culture of human embryonic stem cell-derived cardiomyocytes and rat neonatal cardiac cells. J Mol Cell Cardiol 46:213–224PubMedCrossRef
46.
go back to reference 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:e40PubMedCrossRef 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:e40PubMedCrossRef
47.
go back to reference Shimizu T, Sekine H, Yang J, Isoi Y, Yamato M, Kikuchi A, Kobayashi E, Okano T (2006) Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J 20:708–710PubMed Shimizu T, Sekine H, Yang J, Isoi Y, Yamato M, Kikuchi A, Kobayashi E, Okano T (2006) Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J 20:708–710PubMed
48.
go back to reference Sklansky M (2004) Advances in fetal cardiac imaging. Pediatr Cardiol 25:307–321PubMed Sklansky M (2004) Advances in fetal cardiac imaging. Pediatr Cardiol 25:307–321PubMed
49.
go back to reference Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676PubMedCrossRef Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676PubMedCrossRef
50.
go back to reference Tennstedt C, Chaoui R, Korner H, Dietel M (1999) Spectrum of congenital heart defects and extracardiac malformations associated with chromosomal abnormalities: results of a seven year necropsy study. Heart 82:34–39PubMed Tennstedt C, Chaoui R, Korner H, Dietel M (1999) Spectrum of congenital heart defects and extracardiac malformations associated with chromosomal abnormalities: results of a seven year necropsy study. Heart 82:34–39PubMed
51.
go back to reference Vrana KE, Hipp JD, Goss AM, McCool BA, Riddle DR, Walker SJ, Wettstein PJ, Studer LP, Tabar V, Cunniff K, Chapman K, Vilner L, West MD, Grant KA, Cibelli JB (2003) Nonhuman primate parthenogenetic stem cells. Proc Natl Acad Sci USA 100(Suppl 1):11911–11916PubMedCrossRef Vrana KE, Hipp JD, Goss AM, McCool BA, Riddle DR, Walker SJ, Wettstein PJ, Studer LP, Tabar V, Cunniff K, Chapman K, Vilner L, West MD, Grant KA, Cibelli JB (2003) Nonhuman primate parthenogenetic stem cells. Proc Natl Acad Sci USA 100(Suppl 1):11911–11916PubMedCrossRef
52.
go back to reference Wang Y, Ameer GA, Sheppard BJ, Langer R (2002) A tough biodegradable elastomer. Nat Biotechnol 20:602–606PubMedCrossRef Wang Y, Ameer GA, Sheppard BJ, Langer R (2002) A tough biodegradable elastomer. Nat Biotechnol 20:602–606PubMedCrossRef
53.
go back to reference Wilkins-Haug LE, Benson CB, Tworetzky W, Marshall AC, Jennings RW, Lock JE (2005) In utero intervention for hypoplastic left heart syndrome—a perinatologist’s perspective. Ultrasound Obstet Gynecol 26:481–486PubMedCrossRef Wilkins-Haug LE, Benson CB, Tworetzky W, Marshall AC, Jennings RW, Lock JE (2005) In utero intervention for hypoplastic left heart syndrome—a perinatologist’s perspective. Ultrasound Obstet Gynecol 26:481–486PubMedCrossRef
54.
go back to reference Wobus AM, Wallukat G, Hescheler J (1991) Pluripotent mouse embryonic stem cells are able to differentiate into cardiomyocytes expressing chronotropic responses to adrenergic and cholinergic agents and Ca2+ channel blockers. Differentiation 48:173–182PubMedCrossRef Wobus AM, Wallukat G, Hescheler J (1991) Pluripotent mouse embryonic stem cells are able to differentiate into cardiomyocytes expressing chronotropic responses to adrenergic and cholinergic agents and Ca2+ channel blockers. Differentiation 48:173–182PubMedCrossRef
55.
go back to reference Zandstra PW, Bauwens C, Yin T, Liu Q, Schiller H, Zweigerdt R, Pasumarthi KB, Field LJ (2003) Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng 9:767–778PubMedCrossRef Zandstra PW, Bauwens C, Yin T, Liu Q, Schiller H, Zweigerdt R, Pasumarthi KB, Field LJ (2003) Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng 9:767–778PubMedCrossRef
56.
go back to reference 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 68:106–114PubMedCrossRef 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 68:106–114PubMedCrossRef
57.
go back to reference Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223–230PubMedCrossRef Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223–230PubMedCrossRef
58.
go back to reference Zimmermann WH, Didie M, Doker S, Melnychenko I, Naito H, Rogge C, Tiburcy M, Eschenhagen T (2006) Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 71:419–429PubMedCrossRef Zimmermann WH, Didie M, Doker S, Melnychenko I, Naito H, Rogge C, Tiburcy M, Eschenhagen T (2006) Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 71:419–429PubMedCrossRef
59.
go back to reference Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12:452–458PubMedCrossRef Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12:452–458PubMedCrossRef
60.
go back to reference Zimmermann WH, Eschenhagen T (2007) Embryonic stem cells for cardiac muscle engineering. Trends Cardiovasc Med 17:134–140PubMedCrossRef Zimmermann WH, Eschenhagen T (2007) Embryonic stem cells for cardiac muscle engineering. Trends Cardiovasc Med 17:134–140PubMedCrossRef
Metadata
Title
Cardiac Tissue Engineering: Implications for Pediatric Heart Surgery
Authors
Wolfram-Hubertus Zimmermann
Robert Cesnjevar
Publication date
01-07-2009
Publisher
Springer-Verlag
Published in
Pediatric Cardiology / Issue 5/2009
Print ISSN: 0172-0643
Electronic ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-009-9405-6

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