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Stem Cells International
Volume 2017 (2017), Article ID 8920940, 18 pages
https://doi.org/10.1155/2017/8920940
Review Article

The Rapidly Evolving Concept of Whole Heart Engineering

1Cardiovascular Regenerative Medicine Group, Department of Cardiac, Thoracic and Vascular Surgery, University of Padua, Padua, Italy
2Venetian Institute of Molecular Medicine, Padua, Italy
3Institute of Neuroscience, National Research Council (CNR), Padua, Italy
4Department of Biomedical Sciences, University of Padua and Venetian Institute of Molecular Medicine, Padua, Italy

Correspondence should be addressed to Laura Iop; ti.dpinu@poi.arual

Received 30 June 2017; Accepted 12 September 2017; Published 9 November 2017

Academic Editor: Andrea E. Sprio

Copyright © 2017 Laura Iop et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. Harvey, “De Motu Cordis,” The Circulation of the Blood and Other Writings, translated by Kenneth J. Franklin, p. 1628, 1957. View at Google Scholar
  2. A. P. Ambrosy, M. Gheorghiade, O. Chioncel, R. J. Mentz, and J. Butler, “Global perspectives in hospitalized heart failure: regional and ethnic variation in patient characteristics, management, and outcomes,” Current Heart Failure Reports, vol. 11, no. 4, pp. 416–427, 2014. View at Google Scholar
  3. M. R. Cowie, “The global burden of heart failure,” https://www.escardio.org/static_file/Escardio/Web/Congresses/Slides/Heart%20failure%202015/1183%20-%20The%20global%20burden%20of%20heart%20failure.%20-%20Martin%20COWIE%20(London,%20United%20Kingdom).pdf.
  4. J. Stehlik, J. E. Bavaria, J. Bax et al., “Heart, lung, and vascular registries: evolving goals, successful approaches, and ongoing innovation,” The Journal of Heart and Lung Transplantation, vol. 35, no. 10, pp. 1149–1157, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. S. H. Goldbarg, S. Elmariah, M. A. Miller, and V. Fuster, “Insights into degenerative aortic valve disease,” Journal of the American College of Cardiology, vol. 50, no. 13, pp. 1205–1213, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. K. Singh, T. Humlicek, A. Jeewa, and K. Fester, “Pediatric Cardiac Intensive Care Society 2014 consensus statement,” Pediatric Critical Care Medicine, vol. 17, Supplement 1, no. 3, pp. S69–S76, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. H. C. Ott, T. S. Matthiesen, S.-K. Goh et al., “Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart,” Nature Medicine, vol. 14, no. 2, pp. 213–221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. D. A. Taylor, “From stem cells and cadaveric matrix to engineered organs,” Current Opinion in Biotechnology, vol. 20, no. 5, pp. 598–605, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. P. Jung, D. B. Bhuiyan, and B. M. Ogle, “Solid organ fabrication: comparison of decellularization to 3D bioprinting,” Biomaterials Research, vol. 20, no. 1, p. 27, 2016. View at Publisher · View at Google Scholar
  10. S. F. Badylak and T. W. Gilbert, “Immune response to biologic scaffold materials,” Seminars in Immunology, vol. 20, no. 2, pp. 109–116, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. T. W. Gilbert, T. L. Sellaro, and S. F. Badylak, “Decellularization of tissues and organs,” Biomaterials, vol. 27, no. 19, pp. 3675–3683, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. P. M. Crapo, T. W. Gilbert, and S. F. Badylak, “An overview of tissue and whole organ decellularization processes,” Biomaterials, vol. 32, no. 12, pp. 3233–3243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. O. Langendorff, “Untersuchungen am überlebenden Säugetierherzen,” Pfluegers Archiv, vol. 61, pp. 291–332, 1895. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Yeo, V. Tse, J. Kung et al., “Isolated heart models for studying cardiac electrophysiology: a historical perspective and recent advances,” Journal of Basic and Clinical Physiology and Pharmacology, vol. 28, no. 3, pp. 191–200, 2017. View at Publisher · View at Google Scholar
  15. F. Di Lisa, R. Menabò, R. Barbato, and N. Siliprandi, “Contrasting effects of propionate and propionyl-L-carnitine on energy-linked processes in ischemic hearts,” The American Journal of Physiology, vol. 267, no. 2, Part 2, pp. H455–H461, 1994. View at Google Scholar
  16. H. J. Döring, “The isolated perfused heart according to Langendorff technique--function--application,” Physiologia Bohemoslovaca, vol. 39, no. 6, pp. 481–504, 1990. View at Google Scholar
  17. F. J. Sutherland and D. J. Hearse, “The isolated blood and perfusion fluid perfusion heart,” Pharmacological Research, vol. 41, no. 6, pp. 613–627, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Ytrehus, “The ischemic heart—experimental models,” Pharmacological Research, vol. 42, no. 3, pp. 193–203, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Skrzypiec-Spring, B. Grotthus, A. Szelag, and R. Schulz, “Isolated heart perfusion according to Langendorff—still viable in the new millennium,” Journal of Pharmacological and Toxicological Methods, vol. 55, no. 2, pp. 113–126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. M. A. Dijkman, J. W. Heslinga, P. Sipkema, and N. Westerhof, “Perfusion-induced changes in cardiac O2 consumption and contractility are based on different mechanisms,” The American Journal of Physiology, vol. 271, no. 3, Part 2, pp. H984–H989, 1996. View at Google Scholar
  21. P. Assayag, D. Charlemagne, I. Marty et al., “Effects of sustained low-flow ischemia on myocardial function and calcium-regulating proteins in adult and senescent rat hearts,” Cardiovascular Research, vol. 38, no. 1, pp. 169–180, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. J. M. de Bakker, R. Coronel, S. Tasseron et al., “Ventricular tachycardia in the infarcted, Langendorff-perfused human heart: role of the arrangement of surviving cardiac fibers,” Journal of the American College of Cardiology, vol. 15, no. 7, pp. 1594–1607, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. K. A. Kadipasaoglu, G. W. Bennink, J. L. Conger et al., “An ex vivo model for the reperfusion of explanted human hearts,” Texas Heart Institute Journal, vol. 20, no. 1, pp. 33–39, 1993. View at Google Scholar
  24. P. Akhyari, H. Aubin, P. Gwanmesia et al., “The quest for an optimized protocol for whole-heart decellularization: a comparison of three popular and a novel decellularization technique and their diverse effects on crucial extracellular matrix qualities,” Tissue Engineering Part C: Methods, vol. 17, no. 9, pp. 915–926, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Weymann, S. Loganathan, H. Takahashi et al., “Development and evaluation of a perfusion decellularization porcine heart model—generation of 3-dimensional myocardial neoscaffolds,” Circulation Journal, vol. 75, pp. 852–860, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. J. M. Wainwright, C. A. Czajka, U. B. Patel et al., “Preparation of cardiac extracellular matrix from an intact porcine heart,” Tissue Engineering Part C: Methods, vol. 16, no. 3, pp. 525–532, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Weymann, N. P. Patil, A. Sabashnikov et al., “Bioartificial heart: a human-sized porcine model – the way ahead,” PLoS One, vol. 9, no. 11, article e111591, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. N. T. Remlinger, P. D. Wearden, and T. W. Gilbert, “Procedure for decellularization of porcine heart by retrograde coronary perfusion,” Journal of Visualized Experiments, vol. 6, article e50059, 2012. View at Publisher · View at Google Scholar
  29. N. Merna, C. Robertson, A. La, and S. C. George, “Optical imaging predicts mechanical properties during decellularization of cardiac tissue,” Tissue Engineering Part C: Methods, vol. 19, no. 10, pp. 802–809, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Methe, H. Bäckdahl, B. R. Johansson, N. Nayakawde, G. Dellgren, and S. Sumitran-Holgersson, “An alternative approach to decellularize whole porcine heart,” BioResearch Open Access, vol. 3, no. 6, pp. 327–338, 2014. View at Publisher · View at Google Scholar
  31. N. Momtahan, N. Poornejad, J. A. Struk et al., “Automation of pressure control improves whole porcine heart decellularization,” Tissue Engineering Part C: Methods, vol. 21, no. 11, pp. 1148–1161, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Kitahara, H. Yagi, K. Tajima et al., “Heterotopic transplantation of a decellularized and recellularized whole porcine heart,” Interactive Cardiovascular and Thoracic Surgery, vol. 22, no. 5, pp. 571–579, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. J. P. Guyette, J. M. Charest, R. W. Mills et al., “Bioengineering human myocardium on native extracellular matrix novelty and significance,” Circulation Research, vol. 118, no. 1, pp. 56–72, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. P. L. Sánchez, M. E. Fernández-Santos, M. A. Espinosa et al., “Data from acellular human heart matrix,” Data Brief, vol. 8, pp. 211–219, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Pati, J. Jang, D.-H. Ha et al., “Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink,” Nature Communications, vol. 5, p. 3935, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. S. F. Badylak, “The extracellular matrix as a scaffold for tissue reconstruction,” Seminars in Cell & Developmental Biology, vol. 13, no. 5, pp. 377–383, 2002. View at Google Scholar
  37. M. J. Bissell and J. Aggeler, “Dynamic reciprocity: how do extracellular matrix and hormones direct gene expression?” Progress in Clinical and Biological Research, vol. 249, pp. 251–262, 1987. View at Google Scholar
  38. S. F. Badylak, “The extracellular matrix as a biologic scaffold material,” Biomaterials, vol. 28, no. 25, pp. 3587–3593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” The American Journal of Physiology, vol. 269, no. 2, Part 2, pp. H571–H582, 1995. View at Google Scholar
  40. T. K. Borg and J. B. Caulfield, “The collagen matrix of the heart,” Federation Proceedings, vol. 40, no. 7, pp. 2037–2041, 1981. View at Google Scholar
  41. J. G. Jacot, H. Kita-Matsuo, K. A. Wei et al., “Cardiac myocyte force development during differentiation and maturation,” Annals of the New York Academy of Sciences, vol. 1188, no. 1, pp. 121–127, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Ausoni and S. Sartore, “From fish to amphibians to mammals: in search of novel strategies to optimize cardiac regeneration,” The Journal of Cell Biology, vol. 184, no. 3, pp. 357–364, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. G. K. Zupanc and D. L. Stocum, “Regeneration science needs to broaden its focus to understand why some organisms can regenerate and others not,” Regenerative Medicine, vol. 10, no. 7, pp. 801–803, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Godwin, D. Kuraitis, and N. Rosenthal, “Extracellular matrix considerations for scar-free repair and regeneration: Insights from regenerative diversity among vertebrates,” The International Journal of Biochemistry & Cell Biology, vol. 56, pp. 47–55, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. R. O. Hynes and A. Naba, “Overview of the matrisome--an inventory of extracellular matrix constituents and functions,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 1, article a004903, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Iop, V. Renier, F. Naso et al., “The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds,” Biomaterials, vol. 30, no. 25, pp. 4104–4116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Wu, R. Allen, J. Gao, and Y. Wang, “Artificial niche combining elastomeric substrate and platelets guides vascular differentiation of bone marrow mononuclear cells,” Tissue Engineering Part A, vol. 17, no. 15-16, pp. 1979–1992, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Iop, A. Bonetti, F. Naso et al., “Decellularized allogeneic heart valves demonstrate self-regeneration potential after a long-term preclinical evaluation,” PLoS One, vol. 9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Di Liddo, P. Aguiari, S. Barbon et al., “Nanopatterned acellular valve conduits drive the commitment of blood-derived multipotent cells,” International Journal of Nanomedicine, vol. 11, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Bassat, Y. E. Mutlak, A. Genzelinakh et al., “The extracellular matrix protein Agrin promotes heart regeneration in mice,” Nature, vol. 547, no. 7662, pp. 179–184, 2017. View at Publisher · View at Google Scholar
  51. L. Iop, A. Chiavegato, A. Callegari et al., “Different cardiovascular potential of adult- and fetal-type mesenchymal stem cells in a rat model of heart cryoinjury,” Cell Transplantation, vol. 17, no. 6, pp. 679–694, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Leri, M. Rota, T. Hosoda, P. Goichberg, and P. Anversa, “Cardiac stem cell niches,” Stem Cell Research, vol. 13, no. 3, pp. 631–646, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. K. K. Parker and D. E. Ingber, “Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering,” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, vol. 362, no. 1484, pp. 1267–1279, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Smith, S. Cho, and D. E. Discher, “Mechanosensing of matrix by stem cells: from matrix heterogeneity, contractility, and the nucleus in pore-migration to cardiogenesis and muscle stem cells in vivo,” Seminars in Cell & Developmental Biology, 2017. View at Publisher · View at Google Scholar
  55. K. Forsten-Williams, C. L. Chu, M. Fannon, J. A. Buczek-Thomas, and M. A. Nugent, “Control of growth factor networks by heparan sulfate proteoglycans,” Annals of Biomedical Engineering, vol. 36, no. 12, pp. 2134–2148, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Holley, K. Meade, and C. R. Merry, “Using embryonic stem cells to understand how glycosaminoglycans regulate differentiation,” Biochemical Society Transactions, vol. 42, no. 3, pp. 689–695, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Qiang, S. Y. Lim, M. Lekas et al., “Perlecan heparan sulfate proteoglycan is a critical determinant of angiogenesis in response to mouse hind-limb ischemia,” Canadian Journal of Cardiology, vol. 30, no. 11, pp. 1444–1451, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Williams, K. P. Quinn, I. Georgakoudi, and L. D. Black, “Young developmental age cardiac extracellular matrix promotes the expansion of neonatal cardiomyocytes in vitro,” Acta Biomaterialia, vol. 10, pp. 194–204, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Oberwallner, A. Brodarac, Y. H. Choi et al., “Preparation of cardiac extracellular matrix scaffolds by decellularization of human myocardium,” Journal of Biomedical Materials Research, Part A, vol. 102, pp. 3263–3272, 2014. View at Publisher · View at Google Scholar
  60. K. E. Hatzistergos, H. Quevedo, B. N. Oskouei et al., “Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation,” Circulation Research, vol. 107, pp. 913–922, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Schlosser, C. Dennler, R. Schweizer et al., “Paracrine effects of mesenchymal stem cells enhance vascular regeneration in ischemic murine skin,” Microvascular Research, vol. 83, no. 3, pp. 267–275, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Menasché, “Cell transplantation in myocardium,” Annals of Thoracic Surgery, vol. 75, no. 3, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Rangappa, R. Makkar, and J. Forrester, “Review article: current status of myocardial regeneration: new cell sources and new strategies,” Journal of Cardiovascular Pharmacology and Therapeutics, vol. 15, pp. 338–343, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. K. R. Chien, I. J. Domian, and K. K. Parker, “Cardiogenesis and the complex biology of regenerative cardiovascular medicine,” Science, vol. 322, no. 5907, pp. 1494–1497, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. B. Crawford, S. T. Koshy, G. Jhamb et al., “Cardiac decellularisation with long-term storage and repopulation with canine peripheral blood progenitor cells,” The Canadian Journal of Chemical Engineering, vol. 90, no. 6, pp. 1457–1464, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Pozzobon, S. Bollini, L. Iop et al., “Human bone marrow-derived CD133+ cells delivered to a collagen patch on cryoinjured rat heart promote angiogenesis and arteriogenesis,” Cell Transplantation, vol. 19, no. 10, pp. 1247–1260, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. B.-E. Strauer and G. Steinhoff, “10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart,” Journal of the American College of Cardiology, vol. 58, no. 11, pp. 1095–1104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Bartunek, A. Behfar, D. Dolatabadi et al., “Cardiopoietic stem cell therapy in heart failure: the C-CURE (cardiopoietic stem cell therapy in heart failURE) multicenter randomized trial with lineage-specified biologics,” Journal of the American College of Cardiology, vol. 61, pp. 2329–2338, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Malliaras, R. R. Makkar, R. R. Smith et al., “Intracoronary cardiosphere-derived cells after myocardial infarction,” Journal of the American College of Cardiology, vol. 63, no. 2, pp. 110–122, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. J. H. Houtgraaf, W. K. Den Dekker, B. M. Van Dalen et al., “First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction,” Journal of the American College of Cardiology, vol. 59, no. 5, pp. 539-540, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Takahashi, K. Okita, M. Nakagawa, and S. Yamanaka, “Induction of pluripotent stem cells from fibroblast cultures,” Nature Protocols, vol. 2, no. 12, pp. 3081–3089, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Nakagawa, M. Koyanagi, K. Tanabe et al., “Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts,” Nature Biotechnology, vol. 26, no. 1, pp. 101–106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Y. Kang, J. M. Hong, B. J. Kim, H. J. Cha, and D. W. Cho, “Enhanced endothelialization for developing artificial vascular networks with a natural vessel mimicking the luminal surface in scaffolds,” Acta Biomaterialia, vol. 9, no. 1, pp. 4716–4725, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. M. E. Brown, E. Rondon, D. Rajesh et al., “Derivation of induced pluripotent stem cells from human peripheral blood T lymphocytes,” PLoS One, vol. 5, no. 6, article e11373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. A. J. Rufaihah, N. F. Huang, S. Jamé et al., “Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 11, pp. e72–e79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. N. L. Tulloch, V. Muskheli, M. V. Razumova et al., “Growth of engineered human myocardium with mechanical loading and vascular coculture,” Circulation Research, vol. 109, no. 1, pp. 47–59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Kawamura, S. Miyagawa, K. Miki et al., “Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model,” Circulation, vol. 126, Supplement 1, no. 11, pp. S29–S37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Kawamura, S. Miyagawa, S. Fukushima et al., “Enhanced survival of transplanted human induced pluripotent stem cell-derived cardiomyocytes by the combination of cell sheets with the pedicled omental flap technique in a porcine heart,” Circulation, vol. 128, Supplement 1, no. 11, pp. S87–S94, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. C. B. Jung, A. Moretti, M. Mederos y Schnitzler et al., “Dantrolene rescues arrhythmogenic RYR2 defect in a patient-specific stem cell model of catecholaminergic polymorphic ventricular tachycardia,” EMBO Molecular Medicine, vol. 4, no. 3, pp. 180–191, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. C. L. Mummery, J. Zhang, E. S. Ng, D. A. Elliott, A. G. Elefanty, and T. J. Kamp, “Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview,” Circulation Research, vol. 111, pp. 344–358, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. S. L. J. Ng, K. Narayanan, S. Gao, and A. C. A. Wan, “Lineage restricted progenitors for the repopulation of decellularized heart,” Biomaterials, vol. 32, no. 30, pp. 7571–7580, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. T.-Y. Lu, B. Lin, J. Kim et al., “Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells,” Nature Communications, vol. 4, p. 2307, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. A. T. Naito, I. Shiojima, H. Akazawa et al., “Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 52, pp. 19812–19817, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Ueno, G. Weidinger, T. Osugi et al., “Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 23, pp. 9685–9690, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. S. J. Kattman, A. D. Witty, M. Gagliardi et al., “Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines,” Cell Stem Cell, vol. 8, no. 2, pp. 228–240, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. L. B. Hazeltine, C. S. Simmons, M. R. Salick et al., “Effects of substrate mechanics on contractility of cardiomyocytes generated from human pluripotent stem cells,” International Journal of Cell Biology, vol. 2012, Article ID 508294, 13 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Wang, J. Hao, and C. C. Hong, “Cardiac induction of embryonic stem cells by a small molecule inhibitor of Wnt/beta-catenin signaling,” ACS Chemical Biology, vol. 6, no. 2, pp. 192–197, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. X. Lian, C. Hsiao, G. Wilson et al., “Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 27, pp. E1848–E1857, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Ieda, J.-D. Fu, P. Delgado-Olguin et al., “Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors,” Cell, vol. 142, no. 3, pp. 375–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. J. X. Chen, M. Krane, M.-A. Deutsch et al., “Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5,” Circulation Research, vol. 111, no. 1, pp. 50–55, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Eulalio, M. Mano, M. Dal Ferro et al., “Functional screening identifies miRNAs inducing cardiac regeneration,” Nature, vol. 492, no. 7429, pp. 376–381, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. T. M. Jayawardena, B. Egemnazarov, E. A. Finch et al., “MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes,” Circulation Research, vol. 110, pp. 1465–1473, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Xu, “Turning cardiac fibroblasts into cardiomyocytes in vivo,” Trends in Molecular Medicine, vol. 18, no. 10, pp. 575-576, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Kurotsu, T. Suzuki, and M. Ieda, “Direct reprogramming, epigenetics, and cardiac regeneration,” Journal of Cardiac Failure, vol. 23, no. 7, pp. 552–557, 2017. View at Publisher · View at Google Scholar
  95. S. Ausoni and S. Sartore, “The cardiovascular unit as a dynamic player in disease and regeneration,” Trends in Molecular Medicine, vol. 15, no. 12, pp. 543–552, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. M. J. Robertson, J. L. Dries-Devlin, S. M. Kren, J. S. Burchfield, and D. A. Taylor, “Optimizing recellularization of whole decellularized heart extracellular matrix,” PLoS One, vol. 9, no. 2, article e90406, 2014. View at Google Scholar
  97. C. Muscari, E. Giordano, F. Bonafè, M. Govoni, and C. Guarnieri, “Strategies affording prevascularized cell-based constructs for myocardial tissue engineering,” Stem Cells International, vol. 2014, Article ID 434169, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Schaaf, A. Shibamiya, M. Mewe et al., “Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology,” PLoS One, vol. 6, no. 10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. M. N. Hirt, J. Boeddinghaus, A. Mitchell et al., “Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation,” Journal of Molecular and Cellular Cardiology, vol. 74, pp. 151–161, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Hülsmann, H. Aubin, A. Kranz et al., “A novel customizable modular bioreactor system for whole-heart cultivation under controlled 3D biomechanical stimulation,” Journal of Artificial Organs, vol. 16, no. 3, pp. 294–304, 2013. View at Publisher · View at Google Scholar · View at Scopus
  101. G. Kensah, I. Gruh, J. Viering et al., “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Engineering Part C: Methods, vol. 17, no. 4, pp. 463–473, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. L. Iop, A. Paolin, P. Aguiari, D. Trojan, E. Cogliati, and G. Gerosa, “Decellularized cryopreserved allografts as off-the-shelf allogeneic alternative for heart valve replacement: in vitro assessment before clinical translation,” Journal of Cardiovascular Translational Research, vol. 10, no. 2, pp. 93–103, 2017. View at Publisher · View at Google Scholar
  103. L. Iop and G. Gerosa, “Guided tissue regeneration in heart valve replacement: from preclinical research to first-in-human trials,” BioMed Research International, vol. 2015, Article ID 432901, 13 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. D. K. C. Cooper, M. B. Ezzelarab, H. Hara et al., “The pathobiology of pig-to-primate xenotransplantation: a historical review,” Xenotransplantation, vol. 23, no. 2, pp. 83–105, 2016. View at Publisher · View at Google Scholar · View at Scopus
  105. P. Simon, M. T. Kasimir, G. Seebacher et al., “Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients,” European Journal of Cardio-Thoracic Surgery, vol. 23, no. 6, pp. 1002–1006, 2003. View at Google Scholar
  106. J. I. Spark, S. Yeluri, C. Derham, Y. T. Wong, and D. Leitch, “Incomplete cellular depopulation may explain the high failure rate of bovine ureteric grafts,” The British Journal of Surgery, vol. 95, no. 5, pp. 582–5, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. S. Park, W.-H. Kim, S.-Y. Choi, and Y.-J. Kim, “Removal of alpha-gal epitopes from porcine aortic valve and pericardium using recombinant human alpha galactosidase A,” Journal of Korean Medical Science, vol. 24, no. 6, p. 1126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. K. Choi, J. Shim, N. Ko et al., “Production of heterozygous alpha 1,3-galactosyltransferase (GGTA1) knock-out transgenic miniature pigs expressing human CD39,” Transgenic Research, vol. 26, no. 2, pp. 209–224, 2017. View at Publisher · View at Google Scholar · View at Scopus
  109. E. M. Reuven, S. Leviatan Ben-Arye, T. Marshanski et al., “Characterization of immunogenic Neu5Gc in bioprosthetic heart valves,” Xenotransplantation, vol. 23, no. 5, pp. 381–392, 2016. View at Publisher · View at Google Scholar · View at Scopus
  110. G. W. Byrne, A. M. Azimzadeh, M. Ezzelarab et al., “Histopathologic insights into the mechanism of anti-non-Gal antibody-mediated pig cardiac xenograft rejection,” Xenotransplantation, vol. 20, no. 5, pp. 292–307, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Salama, M. Mosser, X. Lévêque et al., “Neu5Gc and α1-3 GAL xenoantigen knockout does not affect glycemia homeostasis and insulin secretion in pigs,” Diabetes, vol. 66, no. 4, pp. 987–993, 2017. View at Publisher · View at Google Scholar
  112. K. Kallenbach, R. G. Leyh, E. Lefik et al., “Guided tissue regeneration: porcine matrix does not transmit PERV,” Biomaterials, vol. 25, no. 17, pp. 3613–3620, 2004. View at Publisher · View at Google Scholar · View at Scopus
  113. L. Iop and G. Gerosa, “Cutting-edge regenerative medicine technologies for the treatment of heart valve calcification,” in Calcific Aortic Valve Disease, InTech, 2013. View at Publisher · View at Google Scholar
  114. F. van den Akker, S. C. A. de Jager, and J. P. G. Sluijter, “Mesenchymal stem cell therapy for cardiac inflammation: immunomodulatory properties and the influence of Toll-like receptors,” Mediators of Inflammation, vol. 2013, Article ID 181020, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. J. M. Singelyn, J. A. DeQuach, S. B. Seif-Naraghi, R. B. Littlefield, P. J. Schup-Magoffin, and K. L. Christman, “Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering,” Biomaterials, vol. 30, no. 29, pp. 5409–5416, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. R. M. Wang and K. L. Christman, “Decellularized myocardial matrix hydrogels: In basic research and preclinical studies,” Advanced Drug Delivery Reviews, vol. 96, pp. 77–82, 2016. View at Publisher · View at Google Scholar · View at Scopus
  117. K. G. M. Brockbank, K. Schenke-Layland, E. D. Greene et al., “Ice-free cryopreservation of heart valve allografts: better extracellular matrix preservation in vivo and preclinical results,” Cell and Tissue Banking, vol. 13, pp. 663–671, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. M. E. Scarritt, N. C. Pashos, and B. A. Bunnell, “A review of cellularization strategies for tissue engineering of whole organs,” Frontiers in Bioengineering and Biotechnology, vol. 3, p. 43, 2015. View at Publisher · View at Google Scholar