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Constructing biomimetic cardiac tissues: a review of scaffold materials for engineering cardiac patches

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Abstract

Engineered cardiac patches (ECPs) hold great promise to repair ischemia-induced damages to the myocardium. Recent studies have provided robust technological advances in obtaining pure cardiac cell populations as well as various novel scaffold materials to generate engineered cardiac tissues that can significantly improve electrical and contractile functions of damaged myocardium. Given the significance in understanding the cellular and extracellular structural as well as compositional details of native human heart wall, in order to fabricate most suitable scaffold material for cardiac patches, herein, we have reviewed the structure of the human pericardium and heart wall as well as the compositional details of cardiac extracellular matrix (ECM). Moreover, several strategies to obtain cardiac-specific scaffold materials have been reviewed, including natural, synthetic and hybrid hydrogels, electrospun fibers, decellularized native tissues or whole organs, and scaffolds derived from engineered cell sheets. This review provides a comprehensive analysis of different scaffold materials for engineering cardiac tissues.

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References

  1. E.J. Benjamin, S.S. Virani, C.W. Callaway, A.M. Chamberlain, A.R. Chang, S. Cheng, S.E. Chiuve, M. Cushman, F.N. Delling, R. Deo, S.D. de Ferranti, J.F. Ferguson, M. Fornage, C. Gillespie, C.R. Isasi, M.C. Jiménez, L.C. Jordan, S.E. Judd, D. Lackland, J.H. Lichtman, L. Lisabeth, S. Liu, C.T. Longenecker, P.L. Lutsey, J.S. Mackey, D.B. Matchar, K. Matsushita, M.E. Mussolino, K. Nasir, M. O'Flaherty, L.P. Palaniappan, A. Pandey, D.K. Pandey, M.J. Reeves, M.D. Ritchey, C.J. Rodriguez, G.A. Roth, W.D. Rosamond, U.K.A. Sampson, G.M. Satou, S.H. Shah, N.L. Spartano, D.L. Tirschwell, C.W. Tsao, J.H. Voeks, J.Z. Willey, J.T. Wilkins, J.H. Wu, H.M. Alger, S.S. Wong, P. Muntner, American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, Heart disease and stroke statistics-2018 update: a report from the American Heart Association. Circulation 137(12), e67–e492 (2018)

    Article  Google Scholar 

  2. J. Zhang, W. Zhu, M. Radisic, G. Vunjak-Novakovic, Can we engineer a human cardiac patch for therapy? Circ. Res. 123(2), 244–265 (2018a)

    Article  CAS  Google Scholar 

  3. J. Benjamin Emelia et al., Heart disease and stroke statistics—2019 update: a report from the American Heart Association. Circulation 139(10), e56–e528 (2019)

    CAS  Google Scholar 

  4. L. Yue, J. Xie, S. Nattel, Molecular determinants of cardiac fibroblast electrical function and therapeutic implications for atrial fibrillation. Cardiovasc. Res. 89(4), 744–753 (2011)

    Article  CAS  Google Scholar 

  5. B.A. Tompkins, M. Natsumeda, W. Balkan, J.M. Hare, What is the future of cell-based therapy for acute myocardial infarction. Circ. Res. 120(2), 252–255 (2017)

    Article  CAS  Google Scholar 

  6. C.P. Jackman, I.Y. Shadrin, A.L. Carlson, N. Bursac, Human cardiac tissue engineering: from pluripotent stem cells to heart repair. Curr. Opin. Chem. Eng. 7, 57–64 (2015)

    Article  Google Scholar 

  7. P. Menasche et al., Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Eur. Heart J. 36(30), 2011–2017 (2015)

    Article  Google Scholar 

  8. D. Cyranoski, Reprogrammed’ stem cells approved to mend human hearts for the first time. Nature 557, 619–620 (2018)

    Article  CAS  Google Scholar 

  9. T. Ishihara, V.J. Ferrans, M. Jones, S.W. Boyce, O. Kawanami, W.C. Roberts, Histologic and ultrastructural features of normal human parietal pericardium. Am. J. Cardiol. 46(5), 744–753 (1980)

    Article  CAS  Google Scholar 

  10. A.S. Braga-Vilela, E.R. Pimentel, S. Marangoni, M.H. Toyama, B. de Campos Vidal, Extracellular matrix of porcine pericardium: biochemistry and collagen architecture. J. Membr. Biol. 221(1), 15–25 (2008)

    Article  CAS  Google Scholar 

  11. G.A. Gray, I.S. Toor, R.F.P. Castellan, M. Crisan, M. Meloni, Resident cells of the myocardium: more than spectators in cardiac injury, repair and regeneration. Curr. Opin. Physiol. 1, 46–51 (2018)

    Article  CAS  Google Scholar 

  12. W. Zhang et al., Necrotic myocardial cells release damage‐associated molecular patterns that provoke fibroblast activation in vitro and trigger myocardial inflammation and fibrosis in vivo. 4(6), e001993 (2015)

  13. R. Pinto Alexander et al., Revisiting cardiac cellular composition. Circ. Res. 118(3), 400–409 (2016)

    Article  CAS  Google Scholar 

  14. T.D. Johnson, R.C. Hill, M. Dzieciatkowska, V. Nigam, A. Behfar, K.L. Christman, K.C. Hansen, Quantification of decellularized human myocardial matrix: A comparison of six patients. Proteomics Clin. Appl. 10(1), 75–83 (2016)

    Article  CAS  Google Scholar 

  15. D. Bejleri, M.E. Davis, Decellularized extracellular matrix materials for cardiac repair and regeneration. 8(5), 1801217 (2019)

  16. I. Perea-Gil, C. Gálvez-Montón, C. Prat-Vidal, I. Jorba, C. Segú-Vergés, S. Roura, C. Soler-Botija, O. Iborra-Egea, E. Revuelta-López, M.A. Fernández, R. Farré, D. Navajas, A. Bayes-Genis, Head-to-head comparison of two engineered cardiac grafts for myocardial repair: from scaffold characterization to pre-clinical testing. Sci. Rep. 8(1), 6708 (2018)

    Article  CAS  Google Scholar 

  17. E. Bassat, Y.E. Mutlak, A. Genzelinakh, I.Y. Shadrin, K. Baruch Umansky, O. Yifa, D. Kain, D. Rajchman, J. Leach, D. Riabov Bassat, Y. Udi, R. Sarig, I. Sagi, J.F. Martin, N. Bursac, S. Cohen, E. Tzahor, The extracellular matrix protein agrin promotes heart regeneration in mice. Nature 547, 179–184 (2017)

    Article  CAS  Google Scholar 

  18. G. Vunjak-Novakovic, N. Tandon, A. Godier, R. Maidhof, A. Marsano, T.P. Martens, M. Radisic, Challenges in cardiac tissue engineering. Tissue Eng. B Rev. 16(2), 169–187 (2010)

    Article  Google Scholar 

  19. S. Naahidi, M. Jafari, M. Logan, Y. Wang, Y. Yuan, H. Bae, B. Dixon, P. Chen, Biocompatibility of hydrogel-based scaffolds for tissue engineering applications. Biotechnol. Adv. 35(5), 530–544 (2017)

    Article  CAS  Google Scholar 

  20. S. Roura, C. Gálvez-Montón, A. Bayes-Genis, Fibrin, the preferred scaffold for cell transplantation after myocardial infarction? An old molecule with a new life. J. Tissue Eng. Regen. Med. 11(8), 2304–2313 (2017)

    Article  CAS  Google Scholar 

  21. C.P. Jackman, A.M. Ganapathi, H. Asfour, Y. Qian, B.W. Allen, Y. Li, N. Bursac, Engineered cardiac tissue patch maintains structural and electrical properties after epicardial implantation. Biomaterials 159, 48–58 (2018)

    Article  CAS  Google Scholar 

  22. D. Zhang, I.Y. Shadrin, J. Lam, H.Q. Xian, H.R. Snodgrass, N. Bursac, Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34(23), 5813–5820 (2013)

    Article  CAS  Google Scholar 

  23. J.A. Schaefer, et al, A cardiac patch from aligned microvessel and cardiomyocyte patches. 12(2), 546–556 (2018)

  24. I.Y. Shadrin, B.W. Allen, Y. Qian, C.P. Jackman, A.L. Carlson, M.E. Juhas, N. Bursac, Cardiopatch platform enables maturation and scale-up of human pluripotent stem cell-derived engineered heart tissues. Nat. Commun. 8(1), 1825–1825 (2017)

    Article  CAS  Google Scholar 

  25. J.S. Wendel, L. Ye, P. Zhang, R.T. Tranquillo, J.J. Zhang, Functional consequences of a tissue-engineered myocardial patch for cardiac repair in a rat infarct model. Tissue Eng. Part A 20(7–8), 1325–1335 (2014)

    Article  CAS  Google Scholar 

  26. N.J. Kaiser, R.J. Kant, A.J. Minor, K.L.K. Coulombe, Optimizing blended collagen-fibrin hydrogels for cardiac tissue engineering with human iPSC-derived cardiomyocytes. ACS Biomater. Sci. Eng. 5(2), 887–899 (2019)

    Article  CAS  Google Scholar 

  27. Y. Zhang, P. Heher, J. Hilborn, H. Redl, D.A. Ossipov, Hyaluronic acid-fibrin interpenetrating double network hydrogel prepared in situ by orthogonal disulfide cross-linking reaction for biomedical applications. Acta Biomater. 38, 23–32 (2016)

    Article  CAS  Google Scholar 

  28. O. Gsib, J.L. Duval, M. Goczkowski, M. Deneufchatel, O. Fichet, V. Larreta-Garde, S. Bencherif, C. Egles, Evaluation of fibrin-based interpenetrating polymer networks as potential biomaterials for tissue engineering. Nanomaterials 7(12), 436 (2017)

    Article  CAS  Google Scholar 

  29. P. Baei, S. Jalili-Firoozinezhad, S. Rajabi-Zeleti, M. Tafazzoli-Shadpour, H. Baharvand, N. Aghdami, Electrically conductive gold nanoparticle-chitosan thermosensitive hydrogels for cardiac tissue engineering. Mater. Sci. Eng. C 63, 131–141 (2016)

    Article  CAS  Google Scholar 

  30. S.R. Shin, C. Zihlmann, M. Akbari, P. Assawes, L. Cheung, K. Zhang, V. Manoharan, Y.S. Zhang, M. Yüksekkaya, K.T. Wan, M. Nikkhah, M.R. Dokmeci, X.S. Tang, A. Khademhosseini, Reduced graphene oxide-GelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small 12(27), 3677–3689 (2016)

    Article  CAS  Google Scholar 

  31. J.R. Garcia, P.F. Campbell, G. Kumar, J.J. Langberg, L. Cesar, L. Wang, A.J. García, R.D. Levit, A minimally invasive, translational method to deliver hydrogels to the heart through the pericardial space. JACC: Basic Transl. Sci. 2(5), 601–609 (2017)

    Google Scholar 

  32. L. Gao, M.E. Kupfer, J.P. Jung, L. Yang, P. Zhang, Y. da Sie, Q. Tran, V. Ajeti, B.T. Freeman, V.G. Fast, P.J. Campagnola, B.M. Ogle, J. Zhang, Myocardial tissue engineering with cells derived from human-induced pluripotent stem cells and a native-like, high-resolution, 3-dimensionally printed scaffold. Circ. Res. 120(8), 1318–1325 (2017)

    Article  CAS  Google Scholar 

  33. N. Kaneko, R. Matsuda, M. Toda, K. Shimamoto, Three-dimensional reconstruction of the human capillary network and the intramyocardial micronecrosis. Am. J. Physiol. Heart Circ. Physiol. 300(3), H754–H761 (2011)

    Article  CAS  Google Scholar 

  34. T.J. Sill, H.A. von Recum, Electrospinning: applications in drug delivery and tissue engineering. Biomaterials 29(13), 1989–2006 (2008)

    Article  CAS  Google Scholar 

  35. L. Wang, Y. Wu, T. Hu, B. Guo, P.X. Ma, Electrospun conductive nanofibrous scaffolds for engineering cardiac tissue and 3D bioactuators. Acta Biomater. 59, 68–81 (2017)

    Article  CAS  Google Scholar 

  36. Y. Liu, S. Wang, R. Zhang, Composite poly(lactic acid)/chitosan nanofibrous scaffolds for cardiac tissue engineering. Int. J. Biol. Macromol. 103, 1130–1137 (2017)

    Article  CAS  Google Scholar 

  37. A. Elamparithi, A.M. Punnoose, S.F.D. Paul, S. Kuruvilla, Gelatin electrospun nanofibrous matrices for cardiac tissue engineering applications. Int. J. Polym. Mater. Polym. Biomater. 66(1), 20–27 (2017)

    Article  CAS  Google Scholar 

  38. J. Du et al., Potential applications of three-dimensional structure of silk fibroin/poly(ester-urethane) urea nanofibrous scaffold in heart valve tissue engineering. Appl. Surf. Sci. 447, 269–278 (2018)

    Article  CAS  Google Scholar 

  39. M. Suhaeri, R. Subbiah, S.H. Kim, C.H. Kim, S.J. Oh, S.H. Kim, K. Park, Novel platform of cardiomyocyte culture and co-culture via fibroblast-derived matrix-coupled aligned electrospun nanofiber. ACS Appl. Mater. Interfaces 9(1), 224–235 (2017)

    Article  CAS  Google Scholar 

  40. M. Kharaziha, S.R. Shin, M. Nikkhah, S.N. Topkaya, N. Masoumi, N. Annabi, M.R. Dokmeci, A. Khademhosseini, Tough and flexible CNT-polymeric hybrid scaffolds for engineering cardiac constructs. Biomaterials 35(26), 7346–7354 (2014)

    Article  CAS  Google Scholar 

  41. R. Feiner, S. Fleischer, A. Shapira, O. Kalish, T. Dvir, Multifunctional degradable electronic scaffolds for cardiac tissue engineering. J. Control. Release 281, 189–195 (2018)

    Article  CAS  Google Scholar 

  42. R. Arumugam, E.S. Srinadhu, B. Subramanian, S. Nallani, β-PVDF based electrospun nanofibers – a promising material for developing cardiac patches. Med. Hypotheses 122, 31–34 (2019)

    Article  CAS  Google Scholar 

  43. A. D'Amore, T. Yoshizumi, S.K. Luketich, M.T. Wolf, X. Gu, M. Cammarata, R. Hoff, S.F. Badylak, W.R. Wagner, Bi-layered polyurethane – extracellular matrix cardiac patch improves ischemic ventricular wall remodeling in a rat model. Biomaterials 107, 1–14 (2016)

    Article  CAS  Google Scholar 

  44. L. Meier, E.D. Hay, Stimulation of corneal differentiation by interaction between cell surface and extracellular matrix. I. Morphometric analysis of transfilter "induction". J. Cell Biol. 66(2), 275–291 (1975)

    Article  CAS  Google Scholar 

  45. J.W. Holmes, T.K. Borg, J.W. Covell, Structure and mechanics of healing myocardial infarcts. Annu. Rev. Biomed. Eng. 7, 223–253 (2005)

    Article  CAS  Google Scholar 

  46. D. Tirziu, F.J. Giordano, M. Simons, Cell communications in the heart. Circulation 122(9), 928–937 (2010a)

    Article  Google Scholar 

  47. H. Lal et al., Integrins and proximal signaling mechanisms in cardiovascular disease. Front. Biosci. (Landmark Ed.) 14, 2307–2334 (2009)

    Article  CAS  Google Scholar 

  48. M. Asakura, M. Kitakaze, S. Takashima, Y. Liao, F. Ishikura, T. Yoshinaka, H. Ohmoto, K. Node, K. Yoshino, H. Ishiguro, H. Asanuma, S. Sanada, Y. Matsumura, H. Takeda, S. Beppu, M. Tada, M. Hori, S. Higashiyama, Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat. Med. 8(1), 35–40 (2002)

    Article  CAS  Google Scholar 

  49. D.A. Taylor, L.C. Sampaio, Z. Ferdous, A.S. Gobin, L.J. Taite, Decellularized matrices in regenerative medicine. Acta Biomater. 74, 74–89 (2018)

    Article  CAS  Google Scholar 

  50. N. Momtahan, N. Poornejad, J.A. Struk, A.A. Castleton, B.J. Herrod, B.R. Vance, J.P. Eatough, B.L. Roeder, P.R. Reynolds, A.D. Cook, Automation of pressure control improves whole porcine heart decellularization. Tissue Eng. Part C Methods 21(11), 1148–1161 (2015)

    Article  CAS  Google Scholar 

  51. Y. Seo, Y. Jung, S.H. Kim, Decellularized heart ECM hydrogel using supercritical carbon dioxide for improved angiogenesis. Acta Biomater. 67, 270–281 (2018)

    Article  CAS  Google Scholar 

  52. N. Merna, C. Robertson, A. la, S.C. George, Optical imaging predicts mechanical properties during decellularization of cardiac tissue. Tissue Eng. Part C Methods 19(10), 802–809 (2013)

    Article  CAS  Google Scholar 

  53. X. Hong, Y. Yuan, X. Sun, M. Zhou, G. Guo, Q. Zhang, J. Hescheler, J. Xi, Skeletal extracellular matrix supports cardiac differentiation of embryonic stem cells: a potential scaffold for engineered cardiac tissue. Cell. Physiol. Biochem. 45(1), 319–331 (2018a)

    Article  CAS  Google Scholar 

  54. Z. Mosala Nezhad, A. Poncelet, L. de Kerchove, P. Gianello, C. Fervaille, G. el Khoury, Small intestinal submucosa extracellular matrix (CorMatrix®) in cardiovascular surgery: a systematic review. Interact. Cardiovasc. Thorac. Surg. 22(6), 839–850 (2016)

    Article  Google Scholar 

  55. Q. Wang, H. Yang, A. Bai, W. Jiang, X. Li, X. Wang, Y. Mao, C. Lu, R. Qian, F. Guo, T. Ding, H. Chen, S. Chen, J. Zhang, C. Liu, N. Sun, Functional engineered human cardiac patches prepared from nature's platform improve heart function after acute myocardial infarction. Biomaterials 105, 52–65 (2016)

    Article  CAS  Google Scholar 

  56. K. Methe, H. Bäckdahl, B.R. Johansson, N. Nayakawde, G. Dellgren, S. Sumitran-Holgersson, An alternative approach to decellularize whole porcine heart. BioResearch open access 3(6), 327–338 (2014)

    Article  CAS  Google Scholar 

  57. B. Wang et al., Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells. J. Biomed. Mater. Res. Part A 94(4), 1100–1110 (2010)

    Google Scholar 

  58. M. Shah, P. KC, K.M. Copeland, J. Liao, G. Zhang, A thin layer of decellularized porcine myocardium for cell delivery. Sci. Rep. 8(1), 16206–16206 (2018)

    Article  CAS  Google Scholar 

  59. B. Oberwallner, A. Brodarac, P. Anić, T. Šarić, K. Wassilew, K. Neef, Y.H. Choi, C. Stamm, Human cardiac extracellular matrix supports myocardial lineage commitment of pluripotent stem cells. Eur. J. Cardiothorac. Surg. 47(3), 416–425 (2015) discussion 425

    Article  Google Scholar 

  60. E. Garreta, L. de Oñate, M.E. Fernández-Santos, R. Oria, C. Tarantino, A.M. Climent, A. Marco, M. Samitier, E. Martínez, M. Valls-Margarit, R. Matesanz, D.A. Taylor, F. Fernández-Avilés, J.C. Izpisua Belmonte, N. Montserrat, Myocardial commitment from human pluripotent stem cells: rapid production of human heart grafts. Biomaterials 98, 64–78 (2016)

    Article  CAS  Google Scholar 

  61. J.P. Guyette, J.M. Charest, R.W. Mills, B.J. Jank, P.T. Moser, S.E. Gilpin, J.R. Gershlak, T. Okamoto, G. Gonzalez, D.J. Milan, G.R. Gaudette, H.C. Ott, Bioengineering human myocardium on native extracellular matrix. Circ. Res. 118(1), 56–72 (2016)

    Article  CAS  Google Scholar 

  62. H.C. Ott, T.S. Matthiesen, S.K. Goh, L.D. Black, S.M. Kren, T.I. Netoff, D.A. Taylor, Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14(2), 213–221 (2008)

    Article  CAS  Google Scholar 

  63. H. Yasui, J.K. Lee, A. Yoshida, T. Yokoyama, H. Nakanishi, K. Miwa, A.T. Naito, T. Oka, H. Akazawa, J. Nakai, S. Miyagawa, Y. Sawa, Y. Sakata, I. Komuro, Excitation propagation in three-dimensional engineered hearts using decellularized extracellular matrix. Biomaterials 35(27), 7839–7850 (2014)

    Article  CAS  Google Scholar 

  64. M.J. Robertson, J.L. Dries-Devlin, S.M. Kren, J.S. Burchfield, D.A. Taylor, Optimizing recellularization of whole decellularized heart extracellular matrix. PLoS One 9(2), e90406 (2014)

    Article  CAS  Google Scholar 

  65. S. Rajabi, S. Pahlavan, M.K. Ashtiani, H. Ansari, S. Abbasalizadeh, F.A. Sayahpour, F. Varzideh, S. Kostin, N. Aghdami, T. Braun, H. Baharvand, Human embryonic stem cell-derived cardiovascular progenitor cells efficiently colonize in bFGF-tethered natural matrix to construct contracting humanized rat hearts. Biomaterials 154, 99–112 (2018)

    Article  CAS  Google Scholar 

  66. H. Lu, T. Hoshiba, N. Kawazoe, G. Chen, Autologous extracellular matrix scaffolds for tissue engineering. Biomaterials 32(10), 2489–2499 (2011)

    Article  CAS  Google Scholar 

  67. E.G. Schmuck, J.D. Mulligan, R.L. Ertel, N.A. Kouris, B.M. Ogle, A.N. Raval, K.W. Saupe, Cardiac fibroblast-derived 3D extracellular matrix seeded with mesenchymal stem cells as a novel device to transfer cells to the ischemic myocardium. Cardiovasc. Eng. Technol. 5(1), 119–131 (2014)

    Article  Google Scholar 

  68. M. Suhaeri, R. Subbiah, S.Y. van, P. du, I.G. Kim, K. Lee, K. Park, Cardiomyoblast (h9c2) differentiation on tunable extracellular matrix microenvironment. Tissue Eng. A 21(11–12), 1940–1951 (2015)

    Article  CAS  Google Scholar 

  69. F. Pagano et al., Normal versus pathological cardiac fibroblast-derived extracellular matrix differentially modulates cardiosphere-derived cell paracrine properties and commitment. Stem Cells Int. 2017, 7396462–7396462 (2017)

    Article  CAS  Google Scholar 

  70. Sharma, D., J. Chica, and F. Zhao. Mesenchymal stem cells for pre-vascularization of engineered tissues. 2018

    Google Scholar 

  71. S.B. Riemenschneider, D.J. Mattia, J.S. Wendel, J.A. Schaefer, L. Ye, P.A. Guzman, R.T. Tranquillo, Inosculation and perfusion of pre-vascularized tissue patches containing aligned human microvessels after myocardial infarction. Biomaterials 97, 51–61 (2016)

    Article  CAS  Google Scholar 

  72. L. Zhang, Z. Qian, M. Tahtinen, S. Qi, F. Zhao, Prevascularization of natural nanofibrous extracellular matrix for engineering completely biological three-dimensional prevascularized tissues for diverse applications. J. Tissue Eng. Regen. Med. 12(3), e1325–e1336 (2018b)

    Article  CAS  Google Scholar 

  73. L. Chen, Q. Xing, Q. Zhai, M. Tahtinen, F. Zhou, L. Chen, Y. Xu, S. Qi, F. Zhao, Pre-vascularization enhances therapeutic effects of human mesenchymal stem cell sheets in full thickness skin wound repair. Theranostics 7(1), 117–131 (2017)

    Article  CAS  Google Scholar 

  74. L. Chen et al., Protocols for full thickness skin wound repair using prevascularized human mesenchymal stem cell sheet. Methods Mol. Biol. 1879, 187–200 (2019)

    Article  Google Scholar 

  75. D. Sharma, W. Jia, F. Long, S. Pati, Q. Chen, Y. Qyang, B. Lee, C.K. Choi, F. Zhao, Polydopamine and collagen coated micro-grated polydimethylsiloxane for human mesenchymal stem cell culture. Bioactive Mater. 4, 142–150 (2019a)

    Article  Google Scholar 

  76. Q. Xing, C. Vogt, K.W. Leong, F. Zhao, Highly aligned nanofibrous scaffold derived from decellularized human fibroblasts. Adv. Funct. Mater. 24(20), 3027–3035 (2014)

    Article  CAS  Google Scholar 

  77. Z. Qian, D. Sharma, W. Jia, D. Radke, T. Kamp, F. Zhao, Engineering stem cell cardiac patch with microvascular features representative of native myocardium. Theranostics 9(8), 2143–2157 (2019)

    Article  CAS  Google Scholar 

  78. Y.C. Chan, S. Ting, Y.K. Lee, K.M. Ng, J. Zhang, Z. Chen, C.W. Siu, S.K.W. Oh, H.F. Tse, Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells. J. Cardiovasc. Transl. Res. 6(6), 989–999 (2013)

    Article  Google Scholar 

  79. Hern et al., electrical stimulation promotes cardiac differentiation of human induced pluripotent stem cells %. J. Stem. Cells Int. 2016, 12 (2016)

    Google Scholar 

  80. W.L. Stoppel, D.L. Kaplan, L.D. Black 3rd, Electrical and mechanical stimulation of cardiac cells and tissue constructs. Adv. Drug Deliv. Rev. 96, 135–155 (2016)

    Article  CAS  Google Scholar 

  81. J. Herron Todd et al., Extracellular matrix–mediated maturation of human pluripotent stem cell–derived cardiac monolayer structure and electrophysiological function. Circ. Arrhythm. Electrophysiol. 9(4), e003638 (2016)

    CAS  Google Scholar 

  82. L. Ye, Y.H. Chang, Q. Xiong, P. Zhang, L. Zhang, P. Somasundaram, M. Lepley, C. Swingen, L. Su, J.S. Wendel, J. Guo, A. Jang, D. Rosenbush, L. Greder, J.R. Dutton, J. Zhang, T.J. Kamp, D.S. Kaufman, Y. Ge, J. Zhang, Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 15(6), 750–761 (2014)

    Article  CAS  Google Scholar 

  83. R.K. Iyer, D. Odedra, L.L.Y. Chiu, G. Vunjak-Novakovic, M. Radisic, Vascular endothelial growth factor secretion by nonmyocytes modulates connexin-43 levels in cardiac organoids. Tissue Eng. Part A 18(17–18), 1771–1783 (2012)

    Article  CAS  Google Scholar 

  84. Y. Shiba, D. Filice, S. Fernandes, E. Minami, S.K. Dupras, B.V. Biber, P. Trinh, Y. Hirota, J.D. Gold, M. Viswanathan, M.A. Laflamme, Electrical integration of human embryonic stem cell-derived cardiomyocytes in a Guinea pig chronic infarct model. J. Cardiovasc. Pharmacol. Ther. 19(4), 368–381 (2014)

    Article  Google Scholar 

  85. J.J. Chong et al., Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510(7504), 273–277 (2014)

    Article  CAS  Google Scholar 

  86. D. Sharma, D. Ross, G. Wang, W. Jia, S.J. Kirkpatrick, F. Zhao, Upgrading prevascularization in tissue engineering: a review of strategies for promoting highly organized microvascular network formation. Acta Biomater. (2019b)

  87. T. Dvir, A. Kedem, E. Ruvinov, O. Levy, I. Freeman, N. Landa, R. Holbova, M.S. Feinberg, S. Dror, Y. Etzion, J. Leor, S. Cohen, Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc. Natl. Acad. Sci. U. S. A. 106(35), 14990–14995 (2009)

    Article  Google Scholar 

  88. R. Noguchi, K. Nakayama, M. Itoh, K. Kamohara, K. Furukawa, J.I. Oyama, K. Node, S. Morita, Development of a three-dimensional pre-vascularized scaffold-free contractile cardiac patch for treating heart disease. J. Heart Lung Transplant. 35(1), 137–145 (2016)

    Article  Google Scholar 

  89. S.D. Anker, A.J.S. Coats, G. Cristian, D. Dragomir, E. Pusineri, M. Piredda, L. Bettari, R. Dowling, M. Volterrani, B.A. Kirwan, G. Filippatos, J.L. Mas, N. Danchin, S.D. Solomon, R.J. Lee, F. Ahmann, A. Hinson, H.N. Sabbah, D.L. Mann, A prospective comparison of alginate-hydrogel with standard medical therapy to determine impact on functional capacity and clinical outcomes in patients with advanced heart failure (AUGMENT-HF trial). Eur. Heart J. 36(34), 2297–2309 (2015)

    Article  CAS  Google Scholar 

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Funding

This study was supported by the National Institutes of Health (1R15CA202656 and 1R15HL145654-01) and the National Science Foundation (1703570) to FZ. It was also supported by NIH 1U01HL134764-01 to TJK.

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Authors and Affiliations

  1. Department of Biomedical Engineering, Michigan Technological University, Houghton, MI, 49931, USA

    Dhavan Sharma, Morgan Ferguson & Feng Zhao

  2. Stem Cell and Regenerative Medicine Center, University of Wisconsin, Madison, WI, 53705, USA

    Timothy J. Kamp

Authors
  1. Dhavan Sharma
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  2. Morgan Ferguson
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  3. Timothy J. Kamp
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  4. Feng Zhao
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Corresponding author

Correspondence to Feng Zhao.

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Sharma, D., Ferguson, M., Kamp, T.J. et al. Constructing biomimetic cardiac tissues: a review of scaffold materials for engineering cardiac patches. emergent mater. 2, 181–191 (2019). https://doi.org/10.1007/s42247-019-00046-4

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  • DOI: https://doi.org/10.1007/s42247-019-00046-4

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