Emergence of Three Dimensional Printed Cardiac Tissue: Opportunities and Challenges in Cardiovascular Diseases

Author(s): Nitin B. Charbe* , Flavia C. Zacconi , Nikhil Amnerkar , Dinesh Pardhi , Priyank Shukla , Tareq L. Mukattash , Paul A. McCarron , Murtaza M. Tambuwala .

Journal Name: Current Cardiology Reviews

Volume 15 , Issue 3 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Three-dimensional (3D) printing, also known as additive manufacturing, was developed originally for engineering applications. Since its early advancements, there has been a relentless development in enthusiasm for this innovation in biomedical research. It allows for the fabrication of structures with both complex geometries and heterogeneous material properties. Tissue engineering using 3D bio-printers can overcome the limitations of traditional tissue engineering methods. It can match the complexity and cellular microenvironment of human organs and tissues, which drives much of the interest in this technique. However, most of the preliminary evaluations of 3Dprinted tissues and organ engineering, including cardiac tissue, relies extensively on the lessons learned from traditional tissue engineering. In many early examples, the final printed structures were found to be no better than tissues developed using traditional tissue engineering methods. This highlights the fact that 3D bio-printing of human tissue is still very much in its infancy and more work needs to be done to realise its full potential. This can be achieved through interdisciplinary collaboration between engineers, biomaterial scientists and molecular cell biologists. This review highlights current advancements and future prospects for 3D bio-printing in engineering ex vivo cardiac tissue and associated vasculature, such as coronary arteries. In this context, the role of biomaterials for hydrogel matrices and choice of cells are discussed. 3D bio-printing has the potential to advance current research significantly and support the development of novel therapeutics which can improve the therapeutic outcomes of patients suffering fatal cardiovascular pathologies.

Keywords: Cardiac tissue engineering, vasculature network, 3D bio-printing, biomaterials, micro-environment, cardiovascular diseases.

[1]
Ahuja P, Sdek P, Maclellan WR. Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 2007; 87: 521-44.
[2]
Studzinski GP, Harrison LE. Differentiation-related changes in the cell cycle traverse. Int Rev Cytol 1999; 189: 1-58.
[3]
Charbe N, McCarron PA, Tambuwala MM. Three-dimensional bio-printing: A new frontier in oncology research. World J Clin Oncol 2017; 8(1): 21.
[4]
Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol 2014; 32(8): 773-85.
[5]
Mandrycky C, Wang Z, Kim K, et al. 3D bioprinting for engineering complex tissues. Biotechnol Adv 2016; 43(4): 422-34.
[6]
Dababneh AB, Ozbolat IT. Bioprinting technology: A current state-of-the-art review. J Manuf Sci Eng 2014; 136(6): 061016.
[7]
Wolinsky H. Printing organs cell-by-cell: 3-D printing is growing in popularity, but how should we regulate the application of this new technology to health care? EMBO Rep 2014; 15(8): 836-8.
[8]
Cui X, Dean D, Ruggeri ZM, et al. Cell damage evaluation of thermal inkjet printed chinese hamster ovary cells. Biotechnol Bioeng 2010; 106(6): 963-9.
[9]
Zhang X, Zhang Y. Tissue engineering applications of three-dimensional bioprinting. Cell Biochem Biophys 2015; 72(3): 777-82.
[10]
Peltola SM, Melchels FPW, Grijpma DW, et al. A review of rapid prototyping techniques for tissue engineering purposes. Ann Med 2008; 40(4): 268-80.
[11]
Skardal A, Atala A. Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng 2015; 43(3): 730-46.
[12]
Wang J, Goyanes A, Gaisford S, et al. Stereolithographic (SLA) 3D printing of oral modified-release dosage forms. Int J Pharm 2016; 503(1-2): 207-12.
[13]
Dai G, Lee V. Three-dimensional bioprinting and tissue fabrication: Prospects for drug discovery and regenerative medicine. Adv Health Care Technol 2015; 1: 23.
[14]
Lee V, Singh G, Trasatti JP, et al. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods 2014; 20(6): 473-84.
[15]
Caspi O, Lesman A, Basevitch Y, et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 2007; 100(2): 263-72.
[16]
Shimizu T, Sekine H, Yang J, et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J 2006; 20(6): 1-20.
[17]
Sakaguchi K, Shimizu T, Horaguchi S, et al. In vitro engineering of vascularized tissue surrogates. Sci Rep 2013; 3: 1316.
[18]
Kolesky DB, Homan KA, Skylar-Scott MA, et al. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci USA 2016; 113(12): 3179-84.
[19]
Engel FB, Schebesta M, Duong MT, et al. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 2005; 19(10): 1175-87.
[20]
Chaudhry HW, Dashoush NH, Tang H, et al. Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J Biol Chem 2004; 279(34): 35858-66.
[21]
Yeong WY, Sudarmadji N, Yu HY, et al. Porous polycaprolactone scaffold for cardiac tissue engineering fabricated by selective laser sintering. Acta Biomater 2010; 6(6): 2028-34.
[22]
Wang Z, Lee SJ, Cheng HJ, et al. 3D bioprinted functional and contractile cardiac tissue constructs. Acta Biomater 2018; 70: 48-56.
[23]
Maiullari F, Costantini M, Milan M, et al. A multi-cellular 3D bioprinting approach for vascularized heart tissue engineering based on HUVECs and iPSC-derived cardiomyocytes. Sci Rep 2018; 8(1): 1-15.
[24]
Perez-Ilzarbe M, Agbulut O, Pelacho B, et al. Characterization of the paracrine effects of human skeletal myoblasts transplanted in infarcted myocardium. Eur J Heart Fail 2008; 10(11): 1065-72.
[25]
Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003; 100(21): 12313-8.
[26]
Jia W, Gungor-Ozkerim PS, Zhang YS, et al. Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials 2016; 106: 58-68.
[27]
Ong CS, Fukunishi T, Zhang H, et al. Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci Rep 2017; 7(1): 1-11.
[28]
Bejleri D, Streeter BW, Nachlas ALY, et al. A bioprinted cardiac patch composed of cardiac-specific extracellular matrix and progenitor cells for heart repair. Adv Healthc Mater 2018; 7(23): e1800672.
[29]
Izadifar M, Chapman D, Babyn P, et al. UV-assisted 3D bioprinting of nano-reinforced hybrid cardiac patch for myocardial tissue engineering. Tissue Eng Part C Methods 2017; 24(2): 74-88.
[30]
Tijore A, Irvine SA, Sarig U, et al. Contact guidance for cardiac tissue engineering using 3D bioprinted gelatin patterned hydrogel. Biofabrication 2018; 10(2): 025003.
[31]
Zhu K, Shin SR, van Kempen T, et al. Gold nanocomposite bioink for printing 3D cardiac constructs. Adv Funct Mater 2017; 27(12): 1605352.
[32]
Yan Y, Wang X, Pan Y, et al. Fabrication of viable tissue-engineered constructs with 3D cell-assembly technique. Biomaterials 2005; 26(29): 5864-71.
[33]
Kim JJ, Hou L, Huang NF. Vascularization of three-dimensional engineered tissues for regenerative medicine applications. Acta Biomater 2016; 41: 17-26.
[34]
Gershlak JR, Hernandez S, Fontana G, et al. Crossing kingdoms: Using decellularized plants as perfusable tissue engineering scaffolds. Biomaterials 2017; 125: 13-22.
[35]
Kirkpatrick CJ, Fuchs S, Unger RE. Co-culture systems for vascularization - Learning from nature. Adv Drug Deliv Rev 2011; 63(4): 291-9.
[36]
Levenberg S, Rouwkema J, Macdonald M, et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 2005; 23(7): 879-84.
[37]
Blau HM, Banfi A. The well-tempered vessel. Nat Med 2001; 7(5): 532-4.
[38]
Jain RK. Molecular regulation of vessel maturation. Nat Med 2003; 9(6): 685-93.
[39]
Richardson TP, Peters MC, Ennett AB, et al. Polymeric system for dual growth factor delivery. Nat Biotechnol 2001; 19(11): 1029-34.
[40]
Schechner JS, Nath K, Zheng L, et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 2000; 97(16): 9191-6.
[41]
Koike N, Fukumura D, Gralla O, et al. Tissue engineering: Creation of long-lasting blood vessels. Nature 2004; 428(6979): 138-9.
[42]
Yamashita J, Itoh H, Hirashima M, et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000; 408(6808): 92-6.
[43]
Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418(6893): 41-9.
[44]
Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 2005; 307(5706): 58-62.
[45]
Bertassoni LE, Cecconi M, Manoharan V, et al. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 2014; 14(13): 2202-11.
[46]
Xu Y, Hu Y, Liu C, et al. A novel strategy for creating tissue-engineered biomimetic blood vessels using 3D bioprinting technology. Materials 2018; 11(9): 1-15.
[47]
Sarker MD, Naghieh S, Sharma NK, et al. 3D biofabrication of vascular networks for tissue regeneration: A report on recent advances. J Pharm Anal 2018; 8(5): 277-96.
[48]
Schöneberg J, De Lorenzi F, Theek B, et al. Engineering biofunctional in vitro vessel models using a multilayer bioprinting technique. Sci Rep 2018; 8(1): 10430.
[49]
Qi J, Li J, Zheng S, Liu J. A vascular fabrication method based on sacrificial material and spraying process. IOP Conf Ser Mater Sci Eng 2018; 394(2): 022061.
[50]
Hannan EL, Racz MJ, Walford G, et al. Long-term outcomes of coronary-artery bypass grafting versus stent implantation. N Engl J Med 2005; 352(21): 2174-83.
[51]
Dahl SLM, Kypson AP, Lawson JH, et al. Readily available tissue-engineered vascular grafts. Sci Transl Med 2011; 3(68): 1-11.
[52]
Matsuda H, Miyazaki M, Oka Y, et al. A polyurethane vascular access graft and a hybrid polytetrafluoroethylene graft as an arteriovenous fistula for hemodialysis: Comparison with an expanded polytetrafluoroethylene graft. Artif Organs 2003; 27(8): 722-7.
[53]
Van Damme H, Deprez M, Creemers E, et al. Intrinsic structural failure of polyester (Dacron) vascular grafts. A general review. Acta Chir Belg 2005; 105(3): 249-55.
[54]
Gary M, Silver GEK, Stutzman FL, et al. Umbilical vein for aortocoronary bypass. Angiology 1982; 33(7): 450-3.
[55]
Vrandecic MO. New graft for the surgical treatment of small vessel diseases. J Cardiovasc Surg 1987; 28(6): 711-4.
[56]
Perloff LJ, Christie BA, Ketharanathan V, et al. A new replacement for small vessels. Surgery 1981; 89(1): 31-41.
[57]
Tomizawa Y, Moon MR, DeAnda A, et al. Coronary bypass grafting with biological grafts in a canine model Circulation 1994; 90(5 II): II160-6.
[58]
Engbers GH, Feijen J. Current techniques to improve the blood compatibility of biomaterial surfaces. Int J Artif Organs 1991; 14(4): 199-215.
[59]
Brothers TE, Stanley JC, Burkel WE, et al. Small-caliber polyurethane and polytetrafluoroethylene grafts: A comparative study in a canine aortoiliac model. J Biomed Mater Res 1990; 24(6): 761-71.
[60]
Lee JB, Wang X, Faley S, et al. Development of 3D microvascular networks within gelatin hydrogels using thermoresponsive sacrificial microfibers. Adv Healthc Mater 2016; 5(7): 781-5.
[61]
Kolesky DB, Truby RL, Gladman AS, et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 2014; 26(19): 3124-30.
[62]
Wu W, Deconinck A, Lewis JA. Omnidirectional printing of 3D microvascular networks. Adv Mater 2011; 23(24): H178-83.
[63]
Hansen CJ, Wu W, Toohey KS, et al. Self-healing materials with interpenetrating microvascular networks. Adv Mater 2009; 21(41): 4143-7.
[64]
Miller JS, Stevens KR, Yang MT, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012; 11(7): 768-74.
[65]
Kinstlinger IS, Miller JS. 3D-printed fluidic networks as vasculature for engineered tissue. Lab Chip 2016; 16(11): 2025-43.
[66]
Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 2007; 7(6): 720-5.
[67]
Zhao L, Lee VK, Yoo S-S, et al. The integration of 3-D cell printing and mesoscopic fluorescence molecular tomography of vascular constructs within thick hydrogel scaffolds. Biomaterials 2012; 33(21): 5325-32.
[68]
Shengjie Li, Zhuo X, Xiaohong W, et al. Direct fabrication of a hybrid cell/hydrogel construct by a double-nozzle assembling technology. J Bioact Compat Polym 2009; 24(3): 249-65.
[69]
Cui X, Boland T. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 2009; 30(31): 6221-7.
[70]
Yang Y, Urbas A, Gonzalez-Bonet A, et al. A composition-controlled cross-linking resin network through rapid visible-light photo-copolymerization. Polym Chem 2016; 7(31): 5023-30.
[71]
Chen PH, Liao HC, Hsu SH, et al. A novel polyurethane/cellulose fibrous scaffold for cardiac tissue engineering. RSC Adv 2015; 5(9): 6932-9.
[72]
Park H, Radisic M, Lim JO, et al. A novel composite scaffold for cardiac tissue engineering. In Vitro Cell Dev Biol Anim 2005; 41(7): 188-96.
[73]
Pok S, Vitale F, Eichmann SL, et al. Biocompatible carbon nanotube-chitosan scaffold matching the electrical conductivity of the heart. ACS Nano 2014; 8(10): 9822-32.
[74]
Lu WN, Lü SH, Wang HB, et al. Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel. Tissue Eng Part A 2009; 15(6): 1437-47.
[75]
Borriello A, Guarino V, Schiavo L, et al. Optimizing PANi doped electroactive substrates as patches for the regeneration of cardiac muscle. J Mater Sci Mater Med 2011; 22(4): 1053-62.
[76]
Peter MG. Applications and environmental aspects of chitin and chitosan. J Macromol Sci Part A 1995; 32(4): 629-40.
[77]
Lee JH, Lee JY, Yang SH, et al. Carbon nanotube-collagen three-dimensional culture of mesenchymal stem cells promotes expression of neural phenotypes and secretion of neurotrophic factors. Acta Biomater 2014; 10(10): 4425-36.
[78]
Agarwal S, Wendorff JH, Greiner A. Use of electrospinning technique for biomedical applications. Polymer 2008; 49(26): 5603-21.
[79]
Patra C, Talukdar S, Novoyatleva T, et al. Silk protein fibroin from Antheraea mylitta for cardiac tissue engineering. Biomaterials 2012; 33(9): 2673-80.
[80]
Naskar D, Nayak S, Dey T, et al. Non-mulberry silk fibroin influence osteogenesis and osteoblast-macrophage cross talk on titanium based surface. Sci Rep 2014; 4: 1-9.
[81]
Mackay TG, Wheatley DJ, Bernacca GM, et al. New polyurethane heart valve prosthesis: Design, manufacture and evaluation. Biomaterials 1996; 17(19): 1857-63.
[82]
Su WF, Ho CC, Shih TH, et al. Exceptional biocompatibility of 3D fibrous scaffold for cardiac tissue engineering fabricated from biodegradable polyurethane blended with cellulose. Int J Polym Mater Polym Biomater 2016; 65(14): 703-11.
[83]
Guelcher SA. Biodegradable polyurethanes: Synthesis and applications in regenerative medicine. Tissue Eng Part B Rev 2008; 14(1): 3-17.
[84]
Cohen A, Yan QL, Shlomovich A, et al. Novel nitrogen-rich energetic macromolecules based on 3,6-dihydrazinyl-1,2,4,5-tetrazine. RSC Adv 2015; 5(129): 106971-80.
[85]
Fujimoto KL, Tobita K, Merryman WD, et al. An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. J Am Coll Cardiol 2007; 49(23): 2292-300.
[86]
Jockenhoevel S, Zund G, Hoerstrup SP, et al. Fibrin gel -- advantages of a new scaffold in cardiovascular tissue engineering. Eur J Cardiothorac Surg 2001; 19(4): 424-30.
[87]
Cheng EY, Kropp BP. Urologic tissue engineering with small-intestinal submucosa: Potential clinical applications. World J Urol 2000; 18(1): 26-30.
[88]
Kuhn AI, Müller M, Knigge S, et al. Novel blood protein based scaffolds for cardiovascular tissue engineering. Curr Dir Biomed Eng 2016; 2(1): 5-9.
[89]
Wang G, McCain ML, Yang L, et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med 2014; 20(6): 616-23.
[90]
Carrier RL, Rupnick M, Langer R, et al. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 2002; 8(2): 175-88.
[91]
Dvir T, Benishti N, Shachar M, et al. A novel perfusion bioreactor providing a homogenous milieu for tissue regeneration. Tissue Eng 2006; 12(10): 2843-52.
[92]
Radisic M, Marsano A, Maidhof R, et al. Cardiac tissue engineering using perfusion bioreactor systems. Nat Protoc 2008; 3(4): 719-38.
[93]
Masuda S, Shimizu T. Three-dimensional cardiac tissue fabrication based on cell sheet technology. Adv Drug Deliv Rev 2016; 96: 103-9.
[94]
Lu TY, Lin B, Kim J, et al. Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat Commun 2013; 4: 2307.
[95]
Choi YS, Matsuda K, Dusting GJ, et al. Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials 2010; 31(8): 2236-42.
[96]
Levenberg S, Golub JS, Amit M, et al. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2002; 99(7): 4391-6.
[97]
Wu SM, Chien KR, Mummery C. Origins and fates of cardiovascular progenitor cells. Cell 2008; 132(4): 537-43.
[98]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[99]
Pei D, Xu J, Zhuang Q, Tse HF, et al. Induced pluripotent stem cell technology in regenerative medicine and biology. Adv Biochem Eng Biotechnol 2010; 123: 127-41.
[100]
Narazaki G, Uosaki H, Teranishi M, et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 2008; 118(5): 498-506.
[101]
Burridge PW, Keller G, Gold JD, et al. Production of de novo cardiomyocytes: Human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012; 10(1): 16-28.
[102]
Zhang J, Wilson GF, Soerens AG, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009; 104(4): e30-41.
[103]
Van Laake LW, Qian L, Cheng P, et al. Reporter-based isolation of induced pluripotent stem cell-and embryonic stem cell-derived cardiac progenitors reveals limited gene expression variance. Circ Res 2010; 107(3): 340-7.
[104]
Martinez-Fernandez A, Nelson TJ, Ikeda Y, et al. c-MYC independent nuclear reprogramming favors cardiogenic potential of induced pluripotent stem cells. J Cardiovasc Transl Res 2010; 3(1): 13-23.
[105]
Molitch-Hou M. Organovo Delivers its 3D Printed Livers - 3D Printing Industry [Internet]. 3D printing industry. 2014. Available from. http: //3dprintingindustry.com/news/organovo-delivers-its-3d-printed-livers-36648/
[106]
Velasquillo C. Skin 3D bioprinting. Applications in cosmetology. J Cosmet Dermatological Sci Appl 2013; 03(01): 85-9.
[107]
Wang C, Tang Z, Zhao Y, et al. Three-dimensional in vitro cancer models: A short review. Biofabrication 2014; 6(2): 022001.
[108]
Roy A, Saxena V, Pandey LM. 3D printing for cardiovascular tissue engineering: A review. Mater Technol 2018; 33(6): 433-42.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 15
ISSUE: 3
Year: 2019
Page: [188 - 204]
Pages: 17
DOI: 10.2174/1573403X15666190112154710
Price: $58

Article Metrics

PDF: 59
HTML: 3