Skip to main content

Advertisement

Log in

3D Bioprinting Stem Cell Derived Tissues

  • Published:
Cellular and Molecular Bioengineering Aims and scope Submit manuscript

Abstract

Stem cells offer tremendous promise for regenerative medicine as they can become a variety of cell types. They also continuously proliferate, providing a renewable source of cells. Recently, it has been found that 3D printing constructs using stem cells, can generate models representing healthy or diseased tissues, as well as substitutes for diseased and damaged tissues. Here, we review the current state of the field of 3D printing stem cell derived tissues. First, we cover 3D printing technologies and discuss the different types of stem cells used for tissue engineering applications. We then detail the properties required for the bioinks used when printing viable tissues from stem cells. We give relevant examples of such bioprinted tissues, including adipose tissue, blood vessels, bone, cardiac tissue, cartilage, heart valves, liver, muscle, neural tissue, and pancreas. Finally, we provide future directions for improving the current technologies, along with areas of focus for future work to translate these exciting technologies into clinical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. AlGhamdi, K. M., A. Kumar, and N. A. Moussa. Low-level laser therapy: a useful technique for enhancing the proliferation of various cultured cells. Lasers Med. Sci. 27(1):237–249, 2012.

    Google Scholar 

  2. Ali, M., et al. Controlling laser-induced jet formation for bioprinting mesenchymal stem cells with high viability and high resolution. Biofabrication 6(4):045001, 2014.

    Google Scholar 

  3. Anil Kumar, S.A.K., S. Park, Y. Ito, B. Joddar. Photo-crosslinkable furfurl-gelatin as a novel bioink for 3D bioprinting of cardiac tissue. In: Annual Meeting of the BMES, 2017, Phoenix, Arizona, 2017.

  4. AsteriasBiotherapeutics, Asterias Biotherapeutics Announces Dosing of First Patient in New SCiSTAR Clinical Trial Cohort Testing AST-OPC1 in an Expanded Cervical Spinal Cord Injury Patient Population. 2016. Asteriasbiotherapuetics.com.

  5. Bajaj, P., et al. Patterned three-dimensional encapsulation of embryonic stem cells using dielectrophoresis and stereolithography. Adv. Healthc. Mater. 2(3):450–458, 2013.

    Google Scholar 

  6. Bakhshinejad, A. and R. M. D’souza. A brief comparison between available bio-printing methods. In: Biomedical Conference (GLBC), 2015 IEEE Great Lakes. IEEE, 2015.

  7. Bang, O. Y., et al. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol. 57(6):874–882, 2005.

    MathSciNet  Google Scholar 

  8. Bao, X., et al. Chemically-defined albumin-free differentiation of human pluripotent stem cells to endothelial progenitor cells. Stem Cell Res. 15(1):122–129, 2015.

    MathSciNet  Google Scholar 

  9. Barabaschi, G. D., et al. Engineering pre-vascularized scaffolds for bone regeneration. Adv. Exp. Med. Biol. 881:79–94, 2015.

    Google Scholar 

  10. Benjamin, E. J., et al. Heart disease and stroke statistics-2017 update: a report from the American Heart Association. Circulation 135(10):e146–e603, 2017.

    Google Scholar 

  11. Beyer, S., et al. 3D alginate constructs for tissue engineering printed using a coaxial flow focusing microfluidic device. In: Solid-State Sensors, Actuators and Microsystems (TRANSDUCERS & EUROSENSORS XXVII), 2013 Transducers & Eurosensors XXVII: The 17th International Conference on. IEEE, 2013.

  12. Beyer, S.T., et al. System For Additive Manufacturing Of Three-Dimensional Structures And Method For Same. 2016, US Patent 20,160,136,895.

  13. Bhuthalingam, R., et al. Automated robotic dispensing technique for surface guidance and bioprinting of cells. JoVE (Journal of Visualized Experiments) 117:e54604, 2016.

    Google Scholar 

  14. Birla, R. K., Y. Huang, and R. Dennis. Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle. Tissue Eng. 13(9):2239–2248, 2007.

    Google Scholar 

  15. Birla, R. K., et al. Myocardial engineering in vivo: formation and characterization of contractile, vascularized three-dimensional cardiac tissue. Tissue Eng. 11(5–6):803–813, 2005.

    Google Scholar 

  16. Blaeser, A., et al. Controlling shear stress in 3D bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv. Healthc. Mater. 5(3):326–333, 2016.

    Google Scholar 

  17. Boland, T., et al. Application of inkjet printing to tissue engineering. Biotechnol. J. 1(9):910–917, 2006.

    Google Scholar 

  18. Bose, S., S. Vahabzadeh, and A. Bandyopadhyay. Bone tissue engineering using 3D printing. Mater. Today 16(12):496–504, 2013.

    Google Scholar 

  19. Bourget, J.-M. et al. Patterning of endothelial cells and mesenchymal stem cells by laser-assisted bioprinting to study cell migration. BioMed. Res. Int. 2016, 2016

  20. Bsoul, A., et al. Design, microfabrication, and characterization of a moulded PDMS/SU-8 inkjet dispenser for a Lab-on-a-Printer platform technology with disposable microfluidic chip. Lab Chip 16(17):3351–3361, 2016.

    Google Scholar 

  21. Butcher, J. T., G. J. Mahler, and L. A. Hockaday. Aortic valve disease and treatment: the need for naturally engineered solutions. Adv. Drug Deliv. Rev. 63(4–5):242–268, 2011.

    Google Scholar 

  22. Byambaa, B., et al. Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv. Healthc. Mater. 2017. https://doi.org/10.1002/adhm.201700015.

    Google Scholar 

  23. Campos, D. F. D., et al. Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication 5(1):015003, 2012.

    MathSciNet  Google Scholar 

  24. Catros, S., et al. Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication 3(2):025001, 2011.

    Google Scholar 

  25. Chia, H. N., and B. M. Wu. Recent advances in 3D printing of biomaterials. J. Biol. Eng. 9(1):4, 2015.

    MathSciNet  Google Scholar 

  26. Chimene, D., et al. Advanced bioinks for 3D printing: a materials science perspective. Ann. Biomed. Eng. 44(6):2090–2102, 2016.

    Google Scholar 

  27. Choi, Y. J., et al. 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink. Adv. Healthc. Mater. 5(20):2636–2645, 2016.

    Google Scholar 

  28. Collins, S. F. Bioprinting is changing regenerative medicine forever. Stem Cells Dev. 23(S1):79–82, 2014.

    Google Scholar 

  29. Cooper, G. M., et al. Inkjet-based biopatterning of bone morphogenetic protein-2 to spatially control calvarial bone formation. Tissue Eng. Part A 16(5):1749–1759, 2010.

    MathSciNet  Google Scholar 

  30. Costantini, M., et al. 3D bioprinting of BM-MSCs-loaded ECM biomimetic hydrogels for in vitro neocartilage formation. Biofabrication 8(3):035002, 2016.

    Google Scholar 

  31. Costantini, M., et al. Microfluidic-enhanced 3D bioprinting of aligned myoblast-laden hydrogels leads to functionally organized myofibers in vitro and in vivo. Biomaterials 131:98–110, 2017.

    Google Scholar 

  32. Cui, X., et al. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat. Drug Deliv. Formul. 6(2):149–155, 2012.

    Google Scholar 

  33. Cui, H., et al. Biologically inspired smart release system based on 3D bioprinted perfused scaffold for vascularized tissue regeneration. Adv. Sci. 3(8):1600058, 2016.

    Google Scholar 

  34. Das, S., et al. Bioprintable, cell-laden silk fibroingelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater. 11:233–246, 2015.

    Google Scholar 

  35. Datta, P., B. Ayan, and I. T. Ozbolat. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater. 51:1–20, 2017.

    Google Scholar 

  36. De Coppi, P., et al. Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol. 25(1):100, 2007.

    Google Scholar 

  37. Dias, A., et al. Generating size-controlled embryoid bodies using laser direct-write. Biofabrication 6(2):025007, 2014.

    Google Scholar 

  38. Drury, J. L., and D. J. Mooney. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24(24):4337–4351, 2003.

    Google Scholar 

  39. Du, M., et al. 3D bioprinting of BMSC-laden methacrylamide gelatin scaffolds with CBD-BMP2-collagen microfibers. Biofabrication 7(4):044104, 2015.

    Google Scholar 

  40. Duan, B., et al. 3D bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J. Biomed. Mater. Res. Part A 101(5):1255–1264, 2013.

    Google Scholar 

  41. Duchi, S., et al. Handheld co-axial bioprinting: application to in situ surgical cartilage repair. Sci. Rep. 7(1):5837, 2017.

    Google Scholar 

  42. Elbert, D. L. Bottom-up tissue engineering. Curr. Opin. Biotechnol. 22(5):674–680, 2011.

    Google Scholar 

  43. Faulkner-Jones, A., et al. Development of a valve-based cell printer for the formation of human embryonic stem cell spheroid aggregates. Biofabrication 5(1):015013, 2013.

    Google Scholar 

  44. Faulkner-Jones, A., et al. Bioprinting of human pluripotent stem cells and their directed differentiation into hepatocyte-like cells for the generation of mini-livers in 3D. Biofabrication 7(4):044102, 2015.

    Google Scholar 

  45. Fedorovich, N. E., et al. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng. 13(8):1905–1925, 2007.

    Google Scholar 

  46. Fedorovich, N. E., et al. Three-dimensional fiber deposition of cell-laden, viable, patterned constructs for bone tissue printing. Tissue Eng. Part A 14(1):127–133, 2008.

    Google Scholar 

  47. Ferreira, J. N., et al. Three-dimensional bioprinting nanotechnologies towards clinical application of stem cells and their secretome in salivary gland regeneration. Stem Cells Int. 2016:1–9, 2016.

    Google Scholar 

  48. Ferris, C. J., et al. Bio-ink for on-demand printing of living cells. Biomater. Sci. 1(2):224–230, 2013.

    Google Scholar 

  49. Filova, E., et al. Tissue-engineered heart valves. Physiol. Res. 58:S141, 2009.

    Google Scholar 

  50. Forget, A., et al. Mechanically tunable bioink for 3D bioprinting of human cells. Adv. Healthc. Mater. 6:1701021, 2017.

    Google Scholar 

  51. Fraser, J. K., et al. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 24(4):150–154, 2006.

    Google Scholar 

  52. Furtado, S., et al. Positron emission tomography after fetal transplantation in Huntington’s disease. Ann. Neurol. 58(2):331–337, 2005.

    Google Scholar 

  53. Gandaglia, A., et al. Cells, scaffolds and bioreactors for tissue-engineered heart valves: a journey from basic concepts to contemporary developmental innovations. Eur. J. Cardiothorac. Surg. 39(4):523–531, 2011.

    Google Scholar 

  54. Gao, G., and X. Cui. Three-dimensional bioprinting in tissue engineering and regenerative medicine. Biotech. Lett. 38(2):203–211, 2016.

    Google Scholar 

  55. Gao, G., et al. Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol. J. 9(10):1304–1311, 2014.

    Google Scholar 

  56. Gao, G., et al. Improved properties of bone and cartilage tissue from 3D inkjet-bioprinted human mesenchymal stem cells by simultaneous deposition and photocrosslinking in PEG-GelMA. Biotechnol. Lett. 37(11):2349–2355, 2015.

    Google Scholar 

  57. Gao, G., et al. Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol. J. 10(10):1568–1577, 2015.

    Google Scholar 

  58. Gao, F., et al. Mesenchymal stem cells and immunomodulation: current status and future prospects. Cell Death Dis. 7(1):e2062, 2017.

    Google Scholar 

  59. Gao, G., et al. NR2F2 regulates chondrogenesis of human mesenchymal stem cells in bioprinted cartilage. Biotechnol. Bioeng. 114(1):208–216, 2017.

    Google Scholar 

  60. Gao, G., et al. Bioprinting cartilage tissue from mesenchymal stem cells and PEG hydrogel. Methods Mol. Biol. (Clifton, NJ) 1612:391, 2017.

    Google Scholar 

  61. Gilbert, F., et al. Print me an organ? Ethical and regulatory issues emerging from 3D bioprinting in medicine. Sci. Eng. Ethics 24:73–91, 2017.

    Google Scholar 

  62. Gitler, A. D., P. Dhillon, and J. Shorter. Neurodegenerative disease: models, mechanisms, and a new hope. Dis. Models Mech. 10(5):499–502, 2017.

    Google Scholar 

  63. Graham, A. D., et al. High-resolution patterned cellular constructs by droplet-based 3D printing. Sci. Rep. 7(1):7004, 2017.

    Google Scholar 

  64. Griffith, L. G., et al. In vitro organogenesis of liver tissue. Ann. N. Y. Acad. Sci. 831(1):382–397, 1997.

    Google Scholar 

  65. Groll, J., et al. Biofabrication: reappraising the definition of an evolving field. Biofabrication 8(1):013001, 2016.

    Google Scholar 

  66. Gruene, M., et al. Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3(1):015005, 2011.

    Google Scholar 

  67. Gruene, M., et al. Laser printing of three-dimensional multicellular arrays for studies of cellcell and cellenvironment interactions. Tissue Eng. Part C 17(10):973–982, 2011.

    Google Scholar 

  68. Gruene, M., et al. Laser printing of stem cells for biofabrication of scaffold-free autologous grafts. Tissue Eng. Part C 17(1):79–87, 2011.

    Google Scholar 

  69. Gu, Q., et al. Functional 3D neural mini-tissues from printed gel-based bioink and human neural stem cells. Adv. Healthc. Mater. 5(12):1429–1438, 2016.

    Google Scholar 

  70. Gu, Q., et al. 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv. Healthc. Mater. 2017. https://doi.org/10.1002/adhm.201700175.

    Google Scholar 

  71. Guillotin, B., and F. Guillemot. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 29(4):183–190, 2011.

    Google Scholar 

  72. Health, N.I.o., Stem cell basics. Stem Cell Information. http://stemcells.nih.gov/info/basics/basics6.asp, 2009.

  73. Hecker, L., et al. Development of a microperfusion system for the culture of bioengineered heart muscle. ASAIO J. 54(3):284–294, 2008.

    Google Scholar 

  74. Henriksson, I., P. Gatenholm, and D. Hägg. Increased lipid accumulation and adipogenic gene expression of adipocytes in 3D bioprinted nanocellulose scaffolds. Biofabrication 9(1):015022, 2017.

    Google Scholar 

  75. Hinton, T. J., et al. 3D printing PDMS elastomer in a hydrophilic support bath via freeform reversible embedding. ACS Biomater. Sci. Eng. 2(10):1781–1786, 2016.

    Google Scholar 

  76. Hoch, E., G. E. Tovar, and K. Borchers. Bioprinting of artificial blood vessels: current approaches towards a demanding goal. Eur. J. Cardiothorac. Surg. 46(5):767–778, 2014.

    Google Scholar 

  77. Hockaday, L., et al. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 4(3):035005, 2012.

    Google Scholar 

  78. Hockaday, L. A., et al. 3D-printed hydrogel technologies for tissue-engineered heart valves. 3D Print. Addit. Manuf. 1(3):122–136, 2014.

    Google Scholar 

  79. Holmes, B., et al. A synergistic approach to the design, fabrication and evaluation of 3D printed micro and nano featured scaffolds for vascularized bone tissue repair. Nanotechnology 27(6):064001, 2016.

    Google Scholar 

  80. Hsieh, F.-Y., and S.-H. Hsu. 3D bioprinting: a new insight into the therapeutic strategy of neural tissue regeneration. Organogenesis 11(4):153–158, 2015.

    Google Scholar 

  81. Hsieh, F.-Y., H.-H. Lin, and S. Hsu. 3D bioprinting of neural stem cell-laden thermoresponsive biodegradable polyurethane hydrogel and potential in central nervous system repair. Biomaterials 71(Supplement C):48–57, 2015.

    Google Scholar 

  82. Huang, Y. C., L. Khait, and R. K. Birla. Contractile three-dimensional bioengineered heart muscle for myocardial regeneration. J. Biomed. Mater. Res. Part A 80(3):719–731, 2007.

    Google Scholar 

  83. Huang, Y., et al. 3D bioprinting and the current applications in tissue engineering. Biotechnol. J. 2017. https://doi.org/10.1002/biot.201600734.

    Google Scholar 

  84. Huang, C.-T., et al. A graphene–polyurethane composite hydrogel as a potential bioink for 3D bioprinting and differentiation of neural stem cells. J. Mater. Chem. B 5(44):8854–8864, 2017.

    Google Scholar 

  85. Hwang, N. S., et al. Effects of three-dimensional culture and growth factors on the chondrogenic differentiation of murine embryonic stem cells. Stem Cells 24(5):284–291, 2005.

    Google Scholar 

  86. Irvine, S. A., and S. S. Venkatraman. Bioprinting and differentiation of stem cells. Molecules 21(9):1188, 2016.

    Google Scholar 

  87. Jakab, K., et al. Tissue engineering by self-assembly of cells printed into topologically defined structures. Tissue Eng. Part A 14(3):413–421, 2008.

    Google Scholar 

  88. Jakab, K., et al. Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2(2):022001, 2010.

    Google Scholar 

  89. Jang, J., et al. Biomaterials-based 3D cell printing for next-generation therapeutics and diagnostics. Biomaterials 156:88, 2017.

    Google Scholar 

  90. Jia, J., et al. Engineering alginate as bioink for bioprinting. Acta Biomater. 10(10):4323–4331, 2014.

    Google Scholar 

  91. Jia, W., et al. Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials 106:58–68, 2016.

    Google Scholar 

  92. Jones, A. C., et al. Assessment of bone ingrowth into porous biomaterials using MICRO-CT. Biomaterials 28(15):2491–2504, 2007.

    Google Scholar 

  93. Kang, H.-W., et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34(3):312, 2016.

    Google Scholar 

  94. Karande, T. S., J. L. Ong, and C. M. Agrawal. Diffusion in musculoskeletal tissue engineering scaffolds: design issues related to porosity, permeability, architecture, and nutrient mixing. Ann. Biomed. Eng. 32(12):1728–1743, 2004.

    Google Scholar 

  95. Kim, S. S., et al. Survival and function of hepatocytes on a novel three-dimensional synthetic biodegradable polymer scaffold with an intrinsic network of channels. Ann. Surg. 228(1):8, 1998.

    Google Scholar 

  96. Kim, S., et al. Vascularized Tissue Regenerative Engineering Using 3D Bioprinting Technology, 2014.

  97. Kmieć, Z. Cooperation of Liver Cells in Health and Disease. Advances in Anatomy, Embryology and Cell Biology, Vol. 161. Berlin: Springer, 2001.

    Google Scholar 

  98. Koch, L., et al. Laser assisted cell printing. Curr. Pharm. Biotechnol. 14(1):91–97, 2013.

    Google Scholar 

  99. Kolesky, D. B., et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26(19):3124–3130, 2014.

    Google Scholar 

  100. Kolesky, D. B., et al. Three-dimensional bioprinting of thick vascularized tissues. Proc. Natl. Acad. Sci. 113(12):3179–3184, 2016.

    Google Scholar 

  101. Lam, C. X. F., et al. Scaffold development using 3D printing with a starch-based polymer. Mater. Sci. Eng. C 20(1–2):49–56, 2002.

    Google Scholar 

  102. Leberfinger, A. N., et al. Concise review: bioprinting of stem cells for transplantable tissue fabrication. Stem Cells Transl. Med. 6:1940–1948, 2017.

    Google Scholar 

  103. Lee, M., B. M. Wu, and J. C. Dunn. Effect of scaffold architecture and pore size on smooth muscle cell growth. J. Biomed. Mater. Res. A 87(4):1010–1016, 2008.

    Google Scholar 

  104. Lee, W., et al. Three-dimensional bioprinting of rat embryonic neural cells. NeuroReport 20(8):798–803, 2009.

    Google Scholar 

  105. Lee, J. Y., et al. Customized biomimetic scaffolds created by indirect three-dimensional printing for tissue engineering. Biofabrication 5(4):045003, 2013.

    Google Scholar 

  106. Lee, J.-S., et al. 3D printing of composite tissue with complex shape applied to ear regeneration. Biofabrication. 6(2):024103, 2014.

    Google Scholar 

  107. Lee, V. K., et al. Generation of multi-scale vascular network system within 3D hydrogel using 3D bio-printing technology. Cell. Mol. Bioeng. 7(3):460–472, 2014.

    Google Scholar 

  108. Lee, H., et al. Development of liver decellularized extracellular matrix bioink for three-dimensional cell printing-based liver tissue engineering. Biomacromolecules 18(4):1229–1237, 2017.

    Google Scholar 

  109. Lee, S.-J., et al. Fabrication of a highly aligned neural scaffold via a table top stereolithography 3D printing and electrospinning. Tissue Eng. Part A 23(11–12):491–502, 2017.

    Google Scholar 

  110. Lei, M., and X. Wang. Biodegradable polymers and stem cells for bioprinting. Molecules 21(5):539, 2016.

    Google Scholar 

  111. Levato, R., et al. Biofabrication of tissue constructs by 3D bioprinting of cell-laden microcarriers. Biofabrication 6(3):035020, 2014.

    Google Scholar 

  112. Levato, R., et al. The bio in the ink: cartilage regeneration with bioprintable hydrogels and articular cartilage-derived progenitor cells. Acta Biomater. 61:41–53, 2017.

    Google Scholar 

  113. Li, Z., and J. Guan. Hydrogels for cardiac tissue engineering. Polymers 3(2):740–761, 2011.

    MathSciNet  Google Scholar 

  114. Lin, H.-H., et al. Preparation and characterization of a biodegradable polyurethane hydrogel and the hybrid gel with soy protein for 3D cell-laden bioprinting. J. Mater. Chem. B 4(41):6694–6705, 2016.

    Google Scholar 

  115. Lindroos, B., R. Suuronen, and S. Miettinen. The potential of adipose stem cells in regenerative medicine. Stem Cell Rev. Rep. 7(2):269–291, 2011.

    Google Scholar 

  116. Loo, Y., et al. Peptide bioink: self-assembling nanofibrous scaffolds for three-dimensional organotypic cultures. Nano Lett. 15(10):6919–6925, 2015.

    Google Scholar 

  117. Ltd., N.C.C. A Study to Evaluate the Safety and Efficacy of AstroStem in Treatment of Alzheimer’s Disease. https://clinicaltrials.gov/ct2/show/NCT03117738.

  118. Ma, X., et al. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc. Natl. Acad. Sci. 113(8):2206–2211, 2016.

    Google Scholar 

  119. Malda, J., et al. 25th anniversary article: engineering hydrogels for biofabrication. Adv. Mater. 25(36):5011–5028, 2013.

    Google Scholar 

  120. Malizos, K. N., and L. K. Papatheodorou. The healing potential of the periosteum molecular aspects. Injury 36(Suppl 3):S13–S19, 2005.

    Google Scholar 

  121. Mandrycky, C., et al. 3D bioprinting for engineering complex tissues. Biotechnol. Adv. 34(4):422–434, 2016.

    Google Scholar 

  122. Marga, F., et al. Developmental biology and tissue engineering. Birth Defects Res. C 81(4):320–328, 2007.

    Google Scholar 

  123. Mazzini, L., et al. Stem cell treatment in amyotrophic lateral sclerosis. J. Neurol. Sci. 265(1):78–83, 2008.

    Google Scholar 

  124. Melchiorri, A. J., and J. P. Fisher. Bioprinting of blood vessels. In: Essentials of 3D Biofabrication and Translation, edited by A. Atala, and J. J. Yoo. Winston-Salem: Elsevier, 2015, pp. 337–350.

    Google Scholar 

  125. Miao, S., et al. 4D printing smart biomedical scaffolds with novel soybean oil epoxidized acrylate. Sci. Rep. 6:27226, 2016.

    Google Scholar 

  126. Miller, J. S., et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11(9):768, 2012.

    Google Scholar 

  127. Mironov, V., et al. Designer ‘blueprint’for vascular trees: morphology evolution of vascular tissue constructs. Virtual Phys. Prototyp. 4(2):63–74, 2009.

    Google Scholar 

  128. Miura, K., et al. Variation in the safety of induced pluripotent stem cell lines. Nat. Biotechnol. 27(8):743, 2009.

    Google Scholar 

  129. Möller, T., et al. In vivo chondrogenesis in 3D bioprinted human cell-laden hydrogel constructs. Plast. Reconstr. Surg. Global Open 5(2):e1227, 2017.

    Google Scholar 

  130. Munaz, A., et al. Three-dimensional printing of biological matters. J. Sci. 1(1):1–17, 2016.

    Google Scholar 

  131. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32(8):773, 2014.

    Google Scholar 

  132. Nature Reviews Stem Cell Collection. Nature Reviews, 2012.

  133. Nguyen, D., et al. Cartilage tissue engineering by the 3D bioprinting of iPS cells in a nanocellulose/alginate bioink. Sci. Rep. 7(1):658, 2017.

    Google Scholar 

  134. Nirmalanandhan, V. S., and G. S. Sittampalam. Stem cells in drug discovery, tissue engineering, and regenerative medicine: emerging opportunities and challenges. J. Biomol. Screen. 14(7):755–768, 2009.

    Google Scholar 

  135. Noh, S., et al. 3D bioprinting for tissue engineering. In: Clinical Regenerative Medicine in Urology, edited by B. W. Kim. Singapore: Springer, 2018, pp. 105–123.

    Google Scholar 

  136. Nombela-Arrieta, C., J. Ritz, and L. E. Silberstein. The elusive nature and function of mesenchymal stem cells. Nat. Rev. Mol. Cell Biol. 12(2):126, 2011.

    Google Scholar 

  137. Norotte, C., et al. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30(30):5910–5917, 2009.

    Google Scholar 

  138. O’Connell, C. D., et al. Development of the Biopen: a handheld device for surgical printing of adipose stem cells at a chondral wound site. Biofabrication 8(1):015019, 2016.

    Google Scholar 

  139. Ong, C. S., et al. 3D bioprinting using stem cells. Pediatr. Res. 83:223, 2017.

    Google Scholar 

  140. Ong, C. S., et al. Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci. Rep. 7(1):4566, 2017.

    Google Scholar 

  141. Orciani, M., et al. Biofabrication and bone tissue regeneration: cell source, approaches, and challenges. Front. Bioeng. Biotechnol. 5:17, 2017.

    Google Scholar 

  142. Ouyang, L., et al. Three-dimensional bioprinting of embryonic stem cells directs highly uniform embryoid body formation. Biofabrication 7(4):044101, 2015.

    Google Scholar 

  143. Pati, F., et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5:3935, 2014.

    Google Scholar 

  144. Patsch, C., et al. Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells. Nat. Cell Biol. 17(8):994, 2015.

    Google Scholar 

  145. Perez-Castillejos, R. Replication of the 3D architecture of tissues. Mater. Today 13(1–2):32–41, 2010.

    Google Scholar 

  146. Phillippi, J. A., et al. Microenvironments engineered by inkjet bioprinting spatially direct adult stem cells toward muscle- and bone-like subpopulations. Stem Cells 26(1):127–134, 2008.

    Google Scholar 

  147. Poldervaart, M. T., et al. Sustained release of BMP-2 in bioprinted alginate for osteogenicity in mice and rats. PLoS ONE 8(8):e72610, 2013.

    Google Scholar 

  148. Pringle, S., et al. Human salivary gland stem cells functionally restore radiation damaged salivary glands. Stem Cells 34(3):640–652, 2016.

    Google Scholar 

  149. Ravnic, D. J., A. N. Leberfinger, and I. T. Ozbolat. Bioprinting and cellular therapies for type 1 diabetes. Trends Biotechnol. 35:1025, 2017.

    Google Scholar 

  150. Richards, D. J., et al. 3D printing for tissue engineering. Isr. J. Chem. 53(9–10):805–814, 2013.

    Google Scholar 

  151. Rivron, N. C., et al. Tissue assembly and organization: developmental mechanisms in microfabricated tissues. Biomaterials 30(28):4851–4858, 2009.

    Google Scholar 

  152. Saltzman, W. M. Tissue Engineering: Engineering Principles for the Design of Replacement Organs and Tissues. Oxford: Oxford University Press, 2004.

    Google Scholar 

  153. Schubert, C., M. C. Van Langeveld, and L. A. Donoso. Innovations in 3D printing: a 3D overview from optics to organs. Br. J. Ophthalmol. 98(2):159–161, 2014.

    Google Scholar 

  154. Singh, V. K., et al. Induced pluripotent stem cells: applications in regenerative medicine, disease modeling, and drug discovery. Front. Cell Dev. Biol. 3:2, 2015.

    Google Scholar 

  155. Skardal, A., J. Zhang, and G. D. Prestwich. Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 31(24):6173–6181, 2010.

    Google Scholar 

  156. Skardal, A., et al. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl. Med. 1(11):792–802, 2012.

    Google Scholar 

  157. Skarstein, K., et al. Adipose tissue is prominent in salivary glands of Sjögren’s syndrome patients and appears to influence the microenvironment in these organs. Autoimmunity 49(5):338–346, 2016.

    Google Scholar 

  158. Smith, D. M., et al. Precise control of osteogenesis for craniofacial defect repair: the role of direct osteoprogenitor contact in BMP-2-based bioprinting. Ann. Plast. Surg. 69(4):485–488, 2012.

    Google Scholar 

  159. Song, J., and J. R. Millman. Economic 3D-printing approach for transplantation of human stem cell-derived β-like cells. Biofabrication 9(1):015002, 2016.

    Google Scholar 

  160. Stichler, S., et al. Double printing of hyaluronic acid/poly (glycidol) hybrid hydrogels with poly (ε-caprolactone) for MSC chondrogenesis. Biofabrication 9:044108, 2017.

    Google Scholar 

  161. Takahashi, K., and S. Yamanaka. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676, 2006.

    Google Scholar 

  162. Takahashi, K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872, 2007.

    Google Scholar 

  163. Tasoglu, S., and U. Demirci. Bioprinting for stem cell research. Trends Biotechnol. 31(1):10–19, 2013.

    Google Scholar 

  164. Tasoglu, S., et al. Manipulating biological agents and cells in micro-scale volumes for applications in medicine. Chem. Soc. Rev. 42(13):5788–5808, 2013.

    Google Scholar 

  165. Tricomi, B. J., A. D. Dias, and D. T. Corr. Stem cell bioprinting for applications in regenerative medicine. Ann. N. Y. Acad. Sci. 1383(1):115–124, 2016.

    Google Scholar 

  166. Truskey, G. A. Advancing cardiovascular tissue engineering. F1000Research 5:1–10, 2016.

    Google Scholar 

  167. Tsang, V. L., and S. N. Bhatia. Three-dimensional tissue fabrication. Adv. Drug Deliv. Rev. 56(11):1635–1647, 2004.

    Google Scholar 

  168. Tsigkou, O., et al. Engineered vascularized bone grafts. Proc. Natl. Acad. Sci. USA 107(8):3311–3316, 2010.

    Google Scholar 

  169. Tuby, H., L. Maltz, and U. Oron. Low-level laser irradiation (LLLI) promotes proliferation of mesenchymal and cardiac stem cells in culture. Lasers Surg. Med. 39(4):373–378, 2007.

    Google Scholar 

  170. Uusimaa, P., et al. Collagen scar formation after acute myocardial infarction: relationships to infarct size, left ventricular function, and coronary artery patency. Circulation 96(8):2565–2572, 1997.

    Google Scholar 

  171. Venkataramana, N. K., et al. Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson’s disease. Transl. Res. 155(2):62–70, 2010.

    Google Scholar 

  172. Ventola, C. L. Medical applications for 3D printing: current and projected uses. Pharm. Therapeutics 39(10):704, 2014.

    Google Scholar 

  173. Vesely, I. Heart valve tissue engineering. Circ. Res. 97(8):743–755, 2005.

    Google Scholar 

  174. von Bültzingslöwen, I., et al. Salivary dysfunction associated with systemic diseases: systematic review and clinical management recommendations. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 103:S57. e1–S57. e15, 2007.

    Google Scholar 

  175. Wang, X., Y. Yan, and R. Zhang. Rapid prototyping as a tool for manufacturing bioartificial livers. Trends Biotechnol. 25(11):505–513, 2007.

    Google Scholar 

  176. Wang, X. F., et al. Osteogenic differentiation of three-dimensional bioprinted constructs consisting of human adipose-derived stem cells in vitro and in vivo. PLoS ONE 11(6):e0157214, 2016.

    Google Scholar 

  177. Wei, Z., et al. 3D printing scaffold coupled with low level light therapy for neural tissue regeneration. Biofabrication 9(2):025002, 2017.

    Google Scholar 

  178. Wenz, A., et al. Bone matrix production in hydroxyapatite-modified hydrogels suitable for bone bioprinting. Biofabrication 9(4):044103, 2017.

    Google Scholar 

  179. Willerth, S. M., and S. E. Sakiyama-Elbert. Approaches to neural tissue engineering using scaffolds for drug delivery. Adv. Drug Deliv. Rev. 59(4):325–338, 2007.

    Google Scholar 

  180. Williams, S. K., et al. Encapsulation of adipose stromal vascular fraction cells in alginate hydrogel spheroids using a direct-write three-dimensional printing system. BioResearch Open Access 2(6):448–454, 2013.

    Google Scholar 

  181. Wu, J., et al. Biomimetic nanofibrous scaffolds for neural tissue engineering and drug development. Drug Discovery Today 22:1375, 2017.

    Google Scholar 

  182. Wüst, S., R. Müller, and S. Hofmann. Controlled positioning of cells in biomaterials—approaches towards 3D tissue printing. J. Funct. Biomater. 2(3):119–154, 2011.

    Google Scholar 

  183. Wüst, S., et al. Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater. 10(2):630–640, 2014.

    Google Scholar 

  184. Xingliang, D., et al. 3D bioprinted glioma stem cells for brain tumor model and applications of drug susceptibility. Biofabrication 8(4):045005, 2016.

    Google Scholar 

  185. Xu, M., et al. An cell-assembly derived physiological 3D model of the metabolic syndrome, based on adipose-derived stromal cells and a gelatin/alginate/fibrinogen matrix. Biomaterials 31(14):3868–3877, 2010.

    Google Scholar 

  186. Xu, F., et al. Embryonic stem cell bioprinting for uniform and controlled size embryoid body formation. Biomicrofluidics 5(2):022207, 2011.

    Google Scholar 

  187. Xu, T., et al. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials 34(1):130–139, 2013.

    Google Scholar 

  188. Yamanaka, S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10(6):678–684, 2012.

    MathSciNet  Google Scholar 

  189. Yan, Y., et al. Fabrication of viable tissue-engineered constructs with 3D cell-assembly technique. Biomaterials 26(29):5864–5871, 2005.

    MathSciNet  Google Scholar 

  190. Yanez, M., et al. In vivo assessment of printed microvasculature in a bilayer skin graft to treat full-thickness wounds. Tissue Eng. Part A 21(1–2):224–233, 2014.

    Google Scholar 

  191. Yang, J., et al. Development of large-scale size-controlled adult pancreatic progenitor cell clusters by an inkjet-printing technique. ACS Appl. Mater. Interfaces. 7(21):11624–11630, 2015.

    Google Scholar 

  192. Yang, L., et al. Three dimensional printing technology and materials for treatment of elbow fractures. Int. Orthop. 41(11):2381–2387, 2017.

    Google Scholar 

  193. Yipeng, J., et al. Microtissues enhance smooth muscle differentiation and cell viability of hADSCs for three dimensional bioprinting. Front. Physiol. 8:534, 2017.

    Google Scholar 

  194. Yu, Y., et al. Evaluation of cell viability and functionality in vessel-like bioprintable cell-laden tubular channels. J. Biomech. Eng. 135(9):091011, 2013.

    Google Scholar 

  195. Zhang, Y., et al. Characterization of printable cellular micro-fluidic channels for tissue engineering. Biofabrication 5(2):025004, 2013.

    Google Scholar 

  196. Zhou, X., et al. 3D bioprinting a cell-laden bone matrix for breast cancer metastasis study. ACS Appl. Mater. Interfaces. 8(44):30017–30026, 2016.

    Google Scholar 

  197. Zhu, W., B.T. Harris, and L.G. Zhang. Gelatin Methacrylamide Hydrogel with Graphene Nanoplatelets for Neural Cell-Laden 3D Bioprinting. IEEE.

  198. Zhu, W., et al. 3D printed nanocomposite matrix for the study of breast cancer bone metastasis. Nanomed. Nanotechnol. Biol. Med. 12(1):69–79, 2016.

    Google Scholar 

Download references

Acknowledgments

The Willerth lab would like to acknowledge funding from the Stem Cell Network, the Canada Research Chairs program, the NSERC Discovery Grant program, MITACS, and the British Columbia Innovation Council. Dr. Willerth has a collaborative research agreement with Aspect Biosystems. Laura De la vega has received graduate support from MITACS. Dr. Joddar acknowledges NIH BUILD Pilot 8UL1GM118970-02, NIH 1SC2HL134642-01 and the NSF-PREM program (DMR 1205302). Nishat Tasnim acknowledges the Anita Mochen Loya fellowship at UTEP. Matthew Alonzo acknowledges the Eloise E. and Patrick B. Wieland fellowship at UTEP. Schweta Anil Kumar, Laila Abelseth, and Meitham Amereh have no other funding sources to declare outside of those mentioned earlier.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Binata Joddar or Stephanie M. Willerth.

Additional information

Associate Editor Michael R. King oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tasnim, N., De la Vega, L., Anil Kumar, S. et al. 3D Bioprinting Stem Cell Derived Tissues. Cel. Mol. Bioeng. 11, 219–240 (2018). https://doi.org/10.1007/s12195-018-0530-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-018-0530-2

Keywords

Navigation