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Nanobiomaterial Advances in Cardiovascular Tissue Engineering

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Cardiovascular Regenerative Medicine

Abstract

Myocardial infarction (MI) is projected to increase globally in the coming decades. The long-term outlook for patients with ischemic heart injury undergoing current treatment modalities is bleak, due to the lack of regenerative capacity of native heart tissue. Tissue engineering and regenerative medicine have developed numerous strategies to repair or replace injured myocardium. One of the most promising strategies to date is the attempt to engineer tissues and cells at the nanoscale by utilizing nanobiomaterials to mimic the native nanoscale structure of the heart. Nanobiomaterials have proliferated enormously in the past few decades and have great potential for creating biomimetic systems that can replace or repair injured myocardium. Tissue engineering scaffolds with precisely controlled nanotopography, electrically conductive nanomaterials with the potential for mimicking conductive pathways in the heart, and numerous nanocarriers for targeted cardiac drug delivery have now been achieved. In this chapter we review the rationale for engineering biological tissues at the nanoscale as well as recent applications in nanofabrication and nanomedicine for cardiac regeneration.

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References

  1. Dalen JE, Alpert JS, Goldberg RJ, Weinstein RS. The epidemic of the 20th century: coronary heart disease. Am J Med. 2014;127(9):807–12.

    Article  PubMed  Google Scholar 

  2. Holmes JW, Laksman Z, Gepstein L. Making better scar: emerging approaches for modifying mechanical and electrical properties following infarction and ablation. Prog Biophys Mol Biol. 2016;120(1–3):134–48.

    Article  PubMed  Google Scholar 

  3. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H. Evidence for cardiomyocyte renewal in humans. Science. 2009;324(5923):98–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Anderson JL, Morrow DA. Acute myocardial infarction. N Engl J Med. 2017;376(21):2053–64.

    Article  CAS  PubMed  Google Scholar 

  5. Chen Q-Z, Harding SE, Ali NN, Lyon AR, Boccaccini AR. Biomaterials in cardiac tissue engineering: ten years of research survey. Mater Sci Eng R Rep. 2008;59(1–6):1–37.

    Article  CAS  Google Scholar 

  6. Christman KL, Lee RJ. Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol. 2006;48(5):907–13.

    Article  CAS  PubMed  Google Scholar 

  7. van Erven L, Schalij MJ. Amiodarone: an effective antiarrhythmic drug with unusual side effects. Heart. 2010;96(19):1593–600.

    Article  PubMed  CAS  Google Scholar 

  8. Goldhill D. Preventing surgical deaths: critical care and intensive care outreach services in the postoperative period. Br J Anaesth. 2004;95(1):88–94.

    Article  PubMed  Google Scholar 

  9. Rankin JS, Hammill BG, Ferguson TB Jr, Glower DD, O’Brien SM, DeLong ER, Peterson ED, Edwards FH. Determinants of operative mortality in valvular heart surgery. J Thorac Cardiovasc Surg. 2006;131(3):547–57.

    Article  PubMed  Google Scholar 

  10. Tachibana A, Santoso MR, Mahmoudi M, Shukla P, Wang L, Bennett M, Goldstone AB, Wang M, Fukushi M, Ebert AD. Paracrine effects of the pluripotent stem cell-derived cardiac myocytes salvage the injured myocardium. Circ Res. 2017;121(6):e22–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103(11):1204–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tang YL, Zhao Q, Qin X, Shen L, Cheng L, Ge J, Phillips MI. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg. 2005;80(1):229–37.

    Article  PubMed  Google Scholar 

  13. Serpooshan V, Wu SM. Cell Stem Cell. 2014;15(6):671–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tang ZC, Liao W-Y, Tang AC, Tsai S-J, Hsieh PC. The enhancement of endothelial cell therapy for angiogenesis in hindlimb ischemia using hyaluronan. Biomaterials. 2011;32(1):75–86.

    Article  CAS  PubMed  Google Scholar 

  15. Wei X, Yang X, Han Z-P, Qu F-F, Shao L, Shi Y-F. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol Sin. 2013;34(6):747.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell–derived cardiomyocytes. Circ Res. 2014;114(3):511–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Volz A, Piper HM, Siegmund B, Schwartz P. Longevity of adult ventricular rat heart muscle cells in serum-free primary culture. J Mol Cell Cardiol. 1991;23(2):161–73.

    Article  CAS  PubMed  Google Scholar 

  18. Zhang Y, Li T-S, Lee S-T, Wawrowsky KA, Cheng K, Galang G, Malliaras K, Abraham MR, Wang C, Marbán E. Dedifferentiation and proliferation of mammalian cardiomyocytes. PLoS One. 2010;5(9):e12559.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Yamanaka S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell. 2012;10(6):678–84.

    Article  CAS  PubMed  Google Scholar 

  20. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2(4):313–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fijnvandraat AC, van Ginneken AC, de Boer PA, Ruijter JM, Christoffels VM, Moorman AF, Lekanne Deprez RH. Cardiomyocytes derived from embryonic stem cells resemble cardiomyocytes of the embryonic heart tube. Cardiovasc Res. 2003;58(2):399–409.

    Article  CAS  PubMed  Google Scholar 

  22. Swijnenburg R-J, Tanaka M, Vogel H, Baker J, Kofidis T, Gunawan F, Lebl DR, Caffarelli AD, de Bruin JL, Fedoseyeva EV. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation. 2005;112(9 suppl):I-166–72.

    Google Scholar 

  23. Nussbaum J, Minami E, Laflamme MA, Virag JA, Ware CB, Masino A, Muskheli V, Pabon L, Reinecke H, Murry CE. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J. 2007;21(7):1345–57.

    Article  CAS  PubMed  Google Scholar 

  24. Ma D, Wei H, Lu J, Ho S, Zhang G, Sun X, Oh Y, Tan SH, Ng ML, Shim W. Generation of patient-specific induced pluripotent stem cell-derived cardiomyocytes as a cellular model of arrhythmogenic right ventricular cardiomyopathy. Eur Heart J. 2012;34(15):1122–33.

    Article  PubMed  CAS  Google Scholar 

  25. Zhou H, Rao MS. Can cord blood banks transform into induced pluripotent stem cell banks? Cytotherapy. 2015;17(6):756–64.

    Article  PubMed  Google Scholar 

  26. Ehnert S, Glanemann M, Schmitt A, Vogt S, Shanny N, Nussler NC, Stöckle U, Nussler A. The possible use of stem cells in regenerative medicine: dream or reality? Langenbeck’s Arch Surg. 2009;394(6):985–97.

    Article  Google Scholar 

  27. Kim D-H, Lipke EA, Kim P, Cheong R, Thompson S, Delannoy M, Suh K-Y, Tung L, Levchenko A. Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci. 2010;107(2):565–70.

    Article  CAS  PubMed  Google Scholar 

  28. Dalby MJ, Gadegaard N, Oreffo RO. Harnessing nanotopography and integrin–matrix interactions to influence stem cell fate. Nat Mater. 2014;13(6):558.

    Article  CAS  PubMed  Google Scholar 

  29. Murtuza B, Nichol JW, Khademhosseini A. Micro-and nanoscale control of the cardiac stem cell niche for tissue fabrication. Tissue Eng Part B Rev. 2009;15(4):443–54.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Conte LL, Chothia C, Janin J. The atomic structure of protein-protein recognition sites1. J Mol Biol. 1999;285(5):2177–98.

    Article  PubMed  Google Scholar 

  31. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM. Self-renewal and differentiation capacity of young and aged stem cells. Exp Cell Res. 2008;314(9):1937–44.

    Article  CAS  PubMed  Google Scholar 

  32. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, Thomson JA, Kamp TJ. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res. 2009;104(4):e30–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Maherali N, Hochedlinger K. Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell. 2008;3(6):595–605.

    Article  CAS  PubMed  Google Scholar 

  34. Villa-Diaz L, Ross A, Lahann J, Krebsbach P. Concise review: the evolution of human pluripotent stem cell culture: from feeder cells to synthetic coatings. Stem Cells. 2013;31(1):1–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kyttälä A, Moraghebi R, Valensisi C, Kettunen J, Andrus C, Pasumarthy KK, Nakanishi M, Nishimura K, Ohtaka M, Weltner J. Genetic variability overrides the impact of parental cell type and determines iPSC differentiation potential. Stem Cell Rep. 2016;6(2):200–12.

    Article  Google Scholar 

  36. Gherghiceanu M, Barad L, Novak A, Reiter I, Itskovitz-Eldor J, Binah O, Popescu L. Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure. J Cell Mol Med. 2011;15(11):2539–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lundy SD, Zhu W-Z, Regnier M, Laflamme MA. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev. 2013;22(14):1991–2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lian X, Hsiao C, Wilson G, Zhu K, Hazeltine LB, Azarin SM, Raval KK, Zhang J, Kamp TJ, Palecek SP. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci. 2012;109(27):E1848–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hong KU, Li Q-H, Guo Y, Patton NS, Moktar A, Bhatnagar A, Bolli R. A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol. 2013;108(3):346.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Zanganeh S, Hutter G, Spitler R, Lenkov O, Mahmoudi M, Shaw A, Pajarinen JS, Nejadnik H, Goodman S, Moseley M. Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues. Nat Nanotechnol. 2016;11(11):986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tolochko N. History of nanotechnology, Nanoscience and nanotechnology. Encyclopaedia of life Support Systems (EOLSS), Developed under the auspices of the UNESCO, SEolss Published, oxford (2009) p. 3–4.

    Google Scholar 

  42. Webster TJ. Nanomedicine: what’s in a definition? Dove Press; 2006.

    Google Scholar 

  43. Von Hippel A. Molecular engineering. Science. 1956;123(3191):315–7.

    Article  Google Scholar 

  44. Van Noorden R. Chemistry: the trials of new carbon. Nature News. 2011;469(7328):14–6.

    Article  CAS  Google Scholar 

  45. MacDonald RA, Laurenzi BF, Viswanathan G, Ajayan PM, Stegemann JP. Collagen–carbon nanotube composite materials as scaffolds in tissue engineering. J Biomed Mater Res A. 2005;74(3):489–96.

    Article  PubMed  CAS  Google Scholar 

  46. Correa-Duarte MA, Wagner N, Rojas-Chapana J, Morsczeck C, Thie M, Giersig M. Fabrication and biocompatibility of carbon nanotube-based 3D networks as scaffolds for cell seeding and growth. Nano Lett. 2004;4(11):2233–6.

    Article  CAS  Google Scholar 

  47. Shin SR, Jung SM, Zalabany M, Kim K, Zorlutuna P, Kim SB, Nikkhah M, Khabiry M, Azize M, Kong J. Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano. 2013;7(3):2369–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Norman JJ, Desai TA. Methods for fabrication of nanoscale topography for tissue engineering scaffolds. Ann Biomed Eng. 2006;34(1):89–101.

    Article  PubMed  Google Scholar 

  49. Neuman KC, Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods. 2008;5(6):491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lee K-S, Kim RH, Yang D-Y, Park SH. Advances in 3D nano/microfabrication using two-photon initiated polymerization. Prog Polym Sci. 2008;33(6):631–81.

    Article  CAS  Google Scholar 

  51. Rosamond WD. Trends in heart failure incidence in the community. Am Heart Assoc. 2017.

    Google Scholar 

  52. Christiansen MN, Køber L, Weeke P, Vasan RS, Jeppesen JL, Smith JG, Gislason GH, Torp-Pedersen C, Andersson C. Age-specific trends in incidence, mortality, and comorbidities of heart failure in Denmark, 1995 to 2012. Circulation. 2017;135(13):1214–23.

    Article  PubMed  Google Scholar 

  53. Liang H, Upmanyu M, Huang H. Size-dependent elasticity of nanowires: nonlinear effects. Phys Rev B. 2005;71(24):241403.

    Article  CAS  Google Scholar 

  54. Saei AA, Yazdani M, Lohse SE, Bakhtiary Z, Serpooshan V, Ghavami M, Asadian M, Mashaghi S, Dreaden EC, Mashaghi A, Mahmoudi M. Nanoparticle surface functionality dictates cellular and systemic toxicity. Chem Mater. 2017;29(16):6578–95.

    Article  CAS  Google Scholar 

  55. Mengsteab PY, Uto K, Smith AS, Frankel S, Fisher E, Nawas Z, Macadangdang J, Ebara M, Kim D-H. Spatiotemporal control of cardiac anisotropy using dynamic nanotopographic cues. Biomaterials. 2016;86:1–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Jafarkhani M, Salehi Z, Kowsari-Esfahan R, Shokrgozar MA, Mohammadi MR, Rajadas J, Mozafari M. Strategies for directing cells into building functional hearts and parts. Biomater Sci. 2018;6:1664–90.

    Article  CAS  PubMed  Google Scholar 

  57. Li W-J, Jiang YJ, Tuan RS. Cell–Nanofiber-based cartilage tissue engineering using improved cell seeding, growth factor, and bioreactor technologies. Tissue Eng A. 2008;14(5):639–48.

    Article  CAS  Google Scholar 

  58. Zhong S, Zhang Y, Lim CT. Fabrication of large pores in electrospun nanofibrous scaffolds for cellular infiltration: a review. Tissue Eng Part B Rev. 2011;18(2):77–87.

    Article  PubMed  CAS  Google Scholar 

  59. Huijing PA. Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J Biomech. 1999;32(4):329–45.

    Article  CAS  PubMed  Google Scholar 

  60. Parker KK, Ingber DE. Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering. Philos Trans R Soc Lond B Biol Sci. 2007;362(1484):1267–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Borg TK. Development of the connective tissue network in the neonatal hamster heart. Dev Dyn. 1982;165(4):435–43.

    CAS  Google Scholar 

  62. Zhao M, Zhang H, Robinson TF, Factor SM, Sonnenblick EH, Eng C. Profound structural alterations of the extracellular collagen matrix in postischemic dysfunctional (“stunned”) but viable myocardium. J Am Coll Cardiol. 1987;10(6):1322–34.

    Article  CAS  PubMed  Google Scholar 

  63. Moal F, Chappard D, Wang J, Vuillemin E, Michalak-Provost S, Rousselet MC, Oberti F, Cales P. Fractal dimension can distinguish models and pharmacologic changes in liver fibrosis in rats. Hepatology. 2002;36(4):840–9.

    Article  PubMed  Google Scholar 

  64. Goldberger AL. Fractal Electrodynamics of the Heartbeata. Ann N Y Acad Sci. 1990;591(1):402–9.

    Article  CAS  PubMed  Google Scholar 

  65. Monteiro LM, Vasques-Nóvoa F, Ferreira L, Nascimento DS. Restoring heart function and electrical integrity: closing the circuit. NPJ Regen Med. 2017;2(1):9.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Cui Z, Ni NC, Wu J, Du G-Q, He S, Yau TM, Weisel RD, Sung H-W, Li R-K. Polypyrrole-chitosan conductive biomaterial synchronizes cardiomyocyte contraction and improves myocardial electrical impulse propagation. Theranostics. 2018;8(10):2752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Liu Y, Liang X, Wang S, Hu K. Electrospun poly (lactic-co-glycolic acid)/multiwalled carbon nanotube nanofibers for cardiac tissue engineering. J Biomater Tissue Eng. 2016;6(9):719–28.

    Article  Google Scholar 

  68. Shin SR, Zihlmann C, Akbari M, Assawes P, Cheung L, Zhang K, Manoharan V, Zhang YS, Yüksekkaya M, Wan Kt. Reduced graphene oxide-gelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small. 2016;12(27):3677–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Anderson RH, Sanchez-Quintana D, Redmann K, Lunkenheimer PP. How are the myocytes aggregated so as to make up the ventricular mass?, Seminars in Thoracic & Cardiovascular Surgery: Pediatric Cardiac Surgery Annual: Elsevier; 2007. p. 76–86.

    Google Scholar 

  70. Kocica MJ, Corno AF, Carreras-Costa F, Ballester-Rodes M, Moghbel MC, Cueva CN, Lackovic V, Kanjuh VI, Torrent-Guasp F. The helical ventricular myocardial band: global, three-dimensional, functional architecture of the ventricular myocardium. Eur J Cardiothorac Surg. 2006;29(Supplement_1):S21–40.

    Article  PubMed  Google Scholar 

  71. Hunter PJ, Borg TK. Integration from proteins to organs: the physiome project. Nat Rev Mol Cell Biol. 2003;4(3):237.

    Article  CAS  PubMed  Google Scholar 

  72. Sapir Y, Polyak B, Cohen S. Nanomaterials for cardiac tissue engineering, Nanomaterials in Tissue Engineering. Cambridge: Woodhead Publishing Limited; 2013. p. 244–75.

    Book  Google Scholar 

  73. Zhou J, Chen J, Sun H, Qiu X, Mou Y, Liu Z, Zhao Y, Li X, Han Y, Duan C. Engineering the heart: evaluation of conductive nanomaterials for improving implant integration and cardiac function. Sci Rep. 2014;4:3733.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Zhang Y, Tang Y, Wang Y, Zhang L. Nanomaterials for cardiac tissue engineering application. Nano-Micro Lett. 2011;3(4):270–7.

    Article  Google Scholar 

  75. Schwartz MA, Schaller MD, Ginsberg MH. Integrins: emerging paradigms of signal transduction. Annu Rev Cell Dev Biol. 1995;11(1):549–99.

    Article  CAS  PubMed  Google Scholar 

  76. Chibowski E, Jurak M. Comparison of contact angle hysteresis of different probe liquids on the same solid surface. Colloid Polym Sci. 2013;291(2):391–9.

    Article  CAS  PubMed  Google Scholar 

  77. Curtis A. Tutorial on the biology of nanotopography. IEEE Trans Nanobioscience. 2004;3(4):293–5.

    Article  PubMed  Google Scholar 

  78. Harrison RG. On the stereotropism of embryonic cells. Science. 1911;34(870):279–81.

    Article  CAS  PubMed  Google Scholar 

  79. Ebendal T. The relative roles of contact inhibition and contact guidance in orientation of axons extending on aligned collagen fibrils in vitro. Exp Cell Res. 1976;98(1):159–69.

    Article  CAS  PubMed  Google Scholar 

  80. Dunn G, Ebendal T. Contact guidance on oriented collagen gels. Exp Cell Res. 1978;111(2):475–9.

    Article  CAS  PubMed  Google Scholar 

  81. Carter SB. Haptotaxis and the mechanism of cell motility. Nature. 1967;213(5073):256–60.

    Article  CAS  PubMed  Google Scholar 

  82. Dunn G, Heath J. A new hypothesis of contact guidance in tissue cells. Exp Cell Res. 1976;101(1):1–14.

    Article  CAS  PubMed  Google Scholar 

  83. Zhao G, Zhang X, Lu TJ, Xu F. Recent advances in electrospun nanofibrous scaffolds for cardiac tissue engineering. Adv Funct Mater. 2015;25(36):5726–38.

    Article  CAS  Google Scholar 

  84. Pham QP, Sharma U, Mikos AG. Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng. 2006;12(5):1197–211.

    Article  CAS  PubMed  Google Scholar 

  85. Fleischer S, Shapira A, Regev O, Nseir N, Zussman E, Dvir T. Albumin fiber scaffolds for engineering functional cardiac tissues. Biotechnol Bioeng. 2014;111(6):1246–57.

    Article  CAS  PubMed  Google Scholar 

  86. Biggs MJP, Richards RG, Dalby MJ. Nanotopographical modification: a regulator of cellular function through focal adhesions. Nanomedicine. 2010;6(5):619–33.

    Article  CAS  PubMed  Google Scholar 

  87. Goversen B, van der Heyden MA, van Veen TA, de Boer TP. The immature electrophysiological phenotype of iPSC-CMs still hampers in vitro drug screening: special focus on I K1. Pharmacol Ther. 2017;183:127–36.

    Article  PubMed  CAS  Google Scholar 

  88. Fong AH, Romero-López M, Heylman CM, Keating M, Tran D, Sobrino A, Tran AQ, Pham HH, Fimbres C, Gershon PD. Three-dimensional adult cardiac extracellular matrix promotes maturation of human induced pluripotent stem cell-derived cardiomyocytes. Tissue Eng A. 2016;22(15–16):1016–25.

    Article  CAS  Google Scholar 

  89. Teo BKK, Wong ST, Lim CK, Kung TY, Yap CH, Ramagopal Y, Romer LH, Yim EK. Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase. ACS Nano. 2013;7(6):4785–98.

    Article  CAS  PubMed  Google Scholar 

  90. Singelyn JM, DeQuach JA, Seif-Naraghi SB, Littlefield RB, Schup-Magoffin PJ, Christman KL. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials. 2009;30(29):5409–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Lieu DK, Fu J-D, Chiamvimonvat N, Tung KWC, McNerney GP, Huser T, Keller G, Kong C-W, Li RA. Mechanism-based facilitated maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Arrhythm Electrophysiol. 2013; https://doi.org/10.1161/CIRCEP.112.973420.

  92. Lutolf M, Hubbell J. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23(1):47.

    Article  CAS  PubMed  Google Scholar 

  93. Khan M, Xu Y, Hua S, Johnson J, Belevych A, Janssen PM, Gyorke S, Guan J, Angelos MG. Evaluation of changes in morphology and function of human induced pluripotent stem cell derived cardiomyocytes (HiPSC-CMs) cultured on an aligned-nanofiber cardiac patch. PLoS One. 2015;10(5):e0126338.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Carson D, Hnilova M, Yang X, Nemeth CL, Tsui JH, Smith AS, Jiao A, Regnier M, Murry CE, Tamerler C. Nanotopography-induced structural anisotropy and sarcomere development in human cardiomyocytes derived from induced pluripotent stem cells. ACS Appl Mater Interfaces. 2016;8(34):21923–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Abadi PP, Garbern JC, Behzadi S, Hill MJ, Tresback JS, Heydari T, Ejtehadi MR, Ahmed N, Copley E, Aghaverdi H. Engineering of mature human induced pluripotent stem cell-derived cardiomyocytes using substrates with multiscale topography. Adv Funct Mater. 2018;28(19)

    Google Scholar 

  96. Parrag IC, Zandstra PW, Woodhouse KA. Fiber alignment and coculture with fibroblasts improves the differentiated phenotype of murine embryonic stem cell-derived cardiomyocytes for cardiac tissue engineering. Biotechnol Bioeng. 2012;109(3):813–22.

    Article  CAS  PubMed  Google Scholar 

  97. Bonart R, Müller E. Phase separation in urethane elastomers as judged by low-angle X-ray scattering. I. Fundamentals. J Macromol Sci Part B: Phys. 1974;10(1):177–89.

    Article  CAS  Google Scholar 

  98. Dicesare P, Fox WM, Hill MJ, Krishnan GR, Yang S, Sarkar D. Cell-material interactions on biphasic polyurethane matrix. J Biomed Mater Res A. 2013;101(8):2151–63.

    Article  PubMed  CAS  Google Scholar 

  99. Hill MJ, Cheah C, Sarkar D. Interfacial energetics approach for analysis of endothelial cell and segmental polyurethane interactions. Colloids Surf B Biointerfaces. 2016;144:46–56.

    Article  CAS  PubMed  Google Scholar 

  100. Kim D-H, Kim P, Suh KY, Choi SK, Lee SH, Kim B Modulation of adhesion and growth of cardiac myocytes by surface nanotopography, Engineering in Medicine and Biology Society, 2005. IEEE-EMBS 2005. 27th Annual International Conference of the, IEEE, 2006, p. 4091–94.

    Google Scholar 

  101. Martinez E, Engel E, Planell J, Samitier J. Effects of artificial micro-and nano-structured surfaces on cell behaviour. Ann Anat. 2009;191(1):126–35.

    Article  CAS  PubMed  Google Scholar 

  102. Wang P-Y, Yu J, Lin J-H, Tsai W-B. Modulation of alignment, elongation and contraction of cardiomyocytes through a combination of nanotopography and rigidity of substrates. Acta Biomater. 2011;7(9):3285–93.

    Article  CAS  PubMed  Google Scholar 

  103. Hazeltine LB, Badur MG, Lian X, Das A, Han W, Palecek SP. Temporal impact of substrate mechanics on differentiation of human embryonic stem cells to cardiomyocytes. Acta Biomater. 2014;10(2):604–12.

    Article  CAS  PubMed  Google Scholar 

  104. Lisichkin G, Novotortsev RY, Bernadyuk S. Chemically modified oxide surfaces capable of molecular recognition. Colloid J. 2004;66(4):387–99.

    Article  CAS  Google Scholar 

  105. Chen L, Wang X, Lu W, Wu X, Li J. Molecular imprinting: perspectives and applications. Chem Soc Rev. 2016;45(8):2137–211.

    Article  CAS  PubMed  Google Scholar 

  106. Mahmoudi M, Bonakdar S, Shokrgozar MA, Aghaverdi H, Hartmann R, Pick A, Witte G, Parak WJ. Cell-imprinted substrates direct the fate of stem cells. ACS Nano. 2013;7(10):8379–84.

    Article  CAS  PubMed  Google Scholar 

  107. Silva BV, Rodríguez BA, Sales GF, Maria Del Pilar TS, Dutra RF. An ultrasensitive human cardiac troponin T graphene screen-printed electrode based on electropolymerized-molecularly imprinted conducting polymer. Biosens Bioelectron. 2016;77:978–85.

    Article  CAS  PubMed  Google Scholar 

  108. Mashinchian O, Bonakdar S, Taghinejad H, Satarifard V, Heidari M, Majidi M, Sharifi S, Peirovi A, Saffar S, Taghinejad M. Cell-imprinted substrates act as an artificial niche for skin regeneration. ACS Appl Mater Interfaces. 2014;6(15):13280–92.

    Article  CAS  PubMed  Google Scholar 

  109. Moreira FT, Sharma S, Dutra RA, Noronha JP, Cass AE, Sales MGF. Protein-responsive polymers for point-of-care detection of cardiac biomarker. Sensors Actuators B Chem. 2014;196:123–32.

    Article  CAS  Google Scholar 

  110. Sun DM, Liu C, Ren WC, Cheng HM. A review of carbon nanotube-and graphene-based flexible thin-film transistors. Small. 2013;9(8):1188–205.

    Article  CAS  PubMed  Google Scholar 

  111. Jin G, Li K. The electrically conductive scaffold as the skeleton of stem cell niche in regenerative medicine. Mater Sci Eng C. 2014;45:671–81.

    Article  CAS  Google Scholar 

  112. Menaa F, Abdelghani A, Menaa B. Graphene nanomaterials as biocompatible and conductive scaffolds for stem cells: impact for tissue engineering and regenerative medicine. J Tissue Eng Regen Med. 2015;9(12):1321–38.

    Article  CAS  PubMed  Google Scholar 

  113. Harrison BS, Atala A. Carbon nanotube applications for tissue engineering. Biomaterials. 2007;28(2):344–53.

    Article  CAS  PubMed  Google Scholar 

  114. Navaei A, Saini H, Christenson W, Sullivan RT, Ros R, Nikkhah M. Gold nanorod-incorporated gelatin-based conductive hydrogels for engineering cardiac tissue constructs. Acta Biomater. 2016;41:133–46.

    Article  CAS  PubMed  Google Scholar 

  115. Fleischer S, Shevach M, Feiner R, Dvir T. Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues. Nanoscale. 2014;6(16):9410–4.

    Article  CAS  PubMed  Google Scholar 

  116. Saravanan S, Nethala S, Pattnaik S, Tripathi A, Moorthi A, Selvamurugan N. Preparation, characterization and antimicrobial activity of a bio-composite scaffold containing chitosan/nano-hydroxyapatite/nano-silver for bone tissue engineering. Int J Biol Macromol. 2011;49(2):188–93.

    Article  CAS  PubMed  Google Scholar 

  117. Liu S, Navaei A, Meng X, Nikkhah M, Chae J. Wireless passive stimulation of engineered cardiac tissues. ACS Sens. 2017;2(7):1006–12.

    Article  CAS  PubMed  Google Scholar 

  118. Tan Y, Richards D, Xu R, Stewart-Clark S, Mani SK, Borg TK, Menick DR, Tian B, Mei Y. Silicon nanowire-induced maturation of cardiomyocytes derived from human induced pluripotent stem cells. Nano Lett. 2015;15(5):2765–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Tian B, Liu J, Dvir T, Jin L, Tsui JH, Qing Q, Suo Z, Langer R, Kohane DS, Lieber CM. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat Mater. 2012;11(11):986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Hou J, Xie Y, Ji A, Cao A, Fang Y, Shi E. Carbon-nanotube-wrapped spider silks for directed cardiomyocyte growth and electrophysiological detection. ACS Appl Mater Interfaces. 2018;10(8):6793–8.

    Article  CAS  PubMed  Google Scholar 

  121. Dvir T, Timko BP, Brigham MD, Naik SR, Karajanagi SS, Levy O, Jin H, Parker KK, Langer R, Kohane DS. Nanowired three-dimensional cardiac patches. Nat Nanotechnol. 2011;6(11):720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Shevach M, Fleischer S, Shapira A, Dvir T. Gold nanoparticle-decellularized matrix hybrids for cardiac tissue engineering. Nano Lett. 2014;14(10):5792–6.

    Article  CAS  PubMed  Google Scholar 

  123. Samal SK, Goranov V, Dash M, Russo A, Shelyakova T, Graziosi P, Lungaro L, Riminucci A, Uhlarz M, Bañobre-López M. Multilayered magnetic gelatin membrane scaffolds. ACS Appl Mater Interfaces. 2015;7(41):23098–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Martinelli V, Cellot G, Toma FM, Long CS, Caldwell JH, Zentilin L, Giacca M, Turco A, Prato M, Ballerini L. Carbon nanotubes promote growth and spontaneous electrical activity in cultured cardiac myocytes. Nano Lett. 2012;12(4):1831–8.

    Article  CAS  PubMed  Google Scholar 

  125. Wang J, Cui C, Nan H, Yu Y, Xiao Y, Poon E, Yang G, Wang X, Wang C, Li L. Graphene sheet-induced global maturation of cardiomyocytes derived from human induced pluripotent stem cells. ACS Appl Mater Interfaces. 2017;9(31):25929–40.

    Article  CAS  PubMed  Google Scholar 

  126. Wong KK, Cheung SO, Huang L, Niu J, Tao C, Ho CM, Che CM, Tam PK. Further evidence of the anti-inflammatory effects of silver nanoparticles. ChemMedChem. 2009;4(7):1129–35.

    Article  CAS  PubMed  Google Scholar 

  127. Rai M, Yadav A, Gade A. Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv. 2009;27(1):76–83.

    Article  CAS  PubMed  Google Scholar 

  128. Allison S, Ahumada M, Andronic C, McNeill B, Variola F, Griffith M, Ruel M, Hamel V, Liang W, Suuronen EJ. Electroconductive nanoengineered biomimetic hybrid fibers for cardiac tissue engineering. J Mater Chem B. 2017;5(13):2402–6.

    Article  CAS  PubMed  Google Scholar 

  129. Rath G, Hussain T, Chauhan G, Garg T, Goyal AK. Collagen nanofiber containing silver nanoparticles for improved wound-healing applications. J Drug Target. 2016;24(6):520–9.

    Article  CAS  PubMed  Google Scholar 

  130. Hajipour MJ, Fromm KM, Ashkarran AA, Jimenez de Aberasturi D, de Larramendi IR, Rojo T, Serpooshan V, Parak WJ, Mahmoudi M. Antibacterial properties of nanoparticles. Trends Biotechnol. 2012;30(10):499–511.

    Article  CAS  PubMed  Google Scholar 

  131. Mahmoudi M, Serpooshan V. Silver-coated engineered magnetic nanoparticles are promising for the success in the fight against antibacterial resistance threat. ACS Nano. 2012;6(3):2656–64.

    Article  CAS  PubMed  Google Scholar 

  132. Martinelli V, Cellot G, Fabbro A, Bosi S, Mestroni L, Ballerini L. Improving cardiac myocytes performance by carbon nanotubes platforms. Front Physiol. 2013;4:239.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Lovat V, Pantarotto D, Lagostena L, Cacciari B, Grandolfo M, Righi M, Spalluto G, Prato M, Ballerini L. Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett. 2005;5(6):1107–10.

    Article  CAS  PubMed  Google Scholar 

  134. Lee T-J, Park S, Bhang SH, Yoon J-K, Jo I, Jeong G-J, Hong BH, Kim B-S. Graphene enhances the cardiomyogenic differentiation of human embryonic stem cells. Biochem Biophys Res Commun. 2014;452(1):174–80.

    Article  CAS  PubMed  Google Scholar 

  135. Cong H, Pan T. Photopatternable conductive PDMS materials for microfabrication. Adv Funct Mater. 2008;18(13):1912–21.

    Article  CAS  Google Scholar 

  136. Shin SR, Migliori B, Miccoli B, Li YC, Mostafalu P, Seo J, Mandla S, Enrico A, Antona S, Sabarish R. Electrically driven microengineered bioinspired soft robots. Adv Mater. 2018;30(10):1704189.

    Google Scholar 

  137. Lin ZC, McGuire AF, Burridge PW, Matsa E, Lou H-Y, Wu JC, Cui B. Accurate nanoelectrode recording of human pluripotent stem cell-derived cardiomyocytes for assaying drugs and modeling disease. Microsyst Nanoeng. 2017;3:16080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Tavano L, Muzzalupo R. Multi-functional vesicles for cancer therapy: the ultimate magic bullet. Colloids Surf B: Biointerfaces. 2016;147:161–71.

    Article  CAS  PubMed  Google Scholar 

  139. Godin B, Sakamoto JH, Serda RE, Grattoni A, Bouamrani A, Ferrari M. Emerging applications of nanomedicine for the diagnosis and treatment of cardiovascular diseases. Trends Pharmacol Sci. 2010;31(5):199–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Kamaly N, Fredman G, Fojas JJR, Subramanian M, Choi WI, Zepeda K, Vilos C, Yu M, Gadde S, Wu J. Targeted interleukin-10 nanotherapeutics developed with a microfluidic chip enhance resolution of inflammation in advanced atherosclerosis. ACS Nano. 2016;10(5):5280–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Kamaly N, Fredman G, Subramanian M, Gadde S, Pesic A, Cheung L, Fayad ZA, Langer R, Tabas I, Farokhzad OC. Development and in vivo efficacy of targeted polymeric inflammation-resolving nanoparticles. Proc Natl Acad Sci. 2013;110(16):6506–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Han J, Kim B, Shin J-Y, Ryu S, Noh M, Woo J, Park J-S, Lee Y, Lee N, Hyeon T. Iron oxide nanoparticle-mediated development of cellular gap junction crosstalk to improve mesenchymal stem cells’ therapeutic efficacy for myocardial infarction. ACS Nano. 2015;9(3):2805–19.

    Article  CAS  PubMed  Google Scholar 

  143. Mahmoudi M, Tachibana A, Goldstone AB, Woo YJ, Chakraborty P, Lee KR, Foote CS, Piecewicz S, Barrozo JC, Wakeel A. Novel MRI contrast agent from magnetotactic bacteria enables in vivo tracking of iPSC-derived cardiomyocytes. Sci Rep. 2016;6:26960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Cheng K, Shen D, Hensley MT, Middleton R, Sun B, Liu W, De Couto G, Marbán E. Magnetic antibody-linked nanomatchmakers for therapeutic cell targeting. Nat Commun. 2014;5:4880.

    Article  CAS  PubMed  Google Scholar 

  145. Serpooshan V, Sivanesan S, Huang X, Mahmoudi M, Malkovskiy AV, Zhao M, Inayathullah M, Wagh D, Zhang XJ, Metzler S. [Pyr1]-Apelin-13 delivery via nano-liposomal encapsulation attenuates pressure overload-induced cardiac dysfunction. Biomaterials. 2015;37:289–98.

    Article  CAS  PubMed  Google Scholar 

  146. Kuba K, Zhang L, Imai Y, Arab S, Chen M, Maekawa Y, Leschnik M, Leibbrandt A, Markovic M, Schwaighofer J. Impaired heart contractility in Apelin gene–deficient mice associated with aging and pressure overload. Circ Res. 2007;101(4):e32–42.

    Article  CAS  PubMed  Google Scholar 

  147. Japp A, Cruden N, Barnes G, Van Gemeren N, Mathews J, Adamson J, Johnston N, Denvir M, Megson I, Flapan A. Acute cardiovascular effects of apelin in humans: potential role in patients with chronic heart failure. Circulation. 2010;121(16):1818–27.

    Article  CAS  PubMed  Google Scholar 

  148. Jayakumar Rajadas PR-L, Serpooshan V. Compositions and methods for treating cardiovascular and pulmonary diseases and disorders with apelin; 2016.

    Google Scholar 

  149. Ott HC, Matthiesen TS, Goh S-K, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14(2):213.

    Article  CAS  PubMed  Google Scholar 

  150. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V. Time evolution of the nanoparticle protein corona. ACS Nano. 2010;4(7):3623–32.

    Article  CAS  PubMed  Google Scholar 

  151. Hajipour MJ, Laurent S, Aghaie A, Rezaee F, Mahmoudi M. Personalized protein coronas: a “key” factor at the nanobiointerface. Biomater Sci. 2014;2(9):1210–21.

    Article  CAS  PubMed  Google Scholar 

  152. Serpooshan V, Mahmoudi M, Zhao M, Wei K, Sivanesan S, Motamedchaboki K, Malkovskiy AV, Gladstone AB, Cohen JE, Yang PC, Rajadas J, Bernstein D, Woo YJ, Ruiz-Lozano P. Protein corona influences cell-biomaterial interactions in nanostructured tissue engineering scaffolds. Adv Funct Mater. 2015;25(28):4379–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by American Heart Association grant # 17SDG33660925 / P.P.S.S. Abadi /2017.

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Hill, M.J., Mahmoudi, M., Abadi, P.P.S.S. (2019). Nanobiomaterial Advances in Cardiovascular Tissue Engineering. In: Serpooshan, V., Wu, S. (eds) Cardiovascular Regenerative Medicine. Springer, Cham. https://doi.org/10.1007/978-3-030-20047-3_5

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