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3D Bioprinting for Vascularized Tissue Fabrication

  • Additive Manufacturing of Biomaterials, Tissues, and Organs
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

3D bioprinting holds remarkable promise for rapid fabrication of 3D tissue engineering constructs. Given its scalability, reproducibility, and precise multi-dimensional control that traditional fabrication methods do not provide, 3D bioprinting provides a powerful means to address one of the major challenges in tissue engineering: vascularization. Moderate success of current tissue engineering strategies have been attributed to the current inability to fabricate thick tissue engineering constructs that contain endogenous, engineered vasculature or nutrient channels that can integrate with the host tissue. Successful fabrication of a vascularized tissue construct requires synergy between high throughput, high-resolution bioprinting of larger perfusable channels and instructive bioink that promotes angiogenic sprouting and neovascularization. This review aims to cover the recent progress in the field of 3D bioprinting of vascularized tissues. It will cover the methods of bioprinting vascularized constructs, bioink for vascularization, and perspectives on recent innovations in 3D printing and biomaterials for the next generation of 3D bioprinting for vascularized tissue fabrication.

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References

  1. Arai, K., S. Iwanaga, H. Toda, C. Genci, Y. Nishiyama, and M. Nakamura. Three-dimensional inkjet biofabrication based on designed images. Biofabrication 3:034113, 2011.

    Article  PubMed  CAS  Google Scholar 

  2. Auger, F. A., L. Gibot, and D. Lacroix. The pivotal role of vascularization in tissue engineering. Annu Rev Biomed Eng 15:177–200, 2013.

    Article  CAS  PubMed  Google Scholar 

  3. Barron, J. A., P. Wu, H. D. Ladouceur, and B. R. Ringeisen. Biological laser printing: a novel technique for creating heterogeneous 3-dimensional cell patterns. Biomed Microdev 6:139–147, 2004.

    Article  CAS  Google Scholar 

  4. Bertassoni, L. E., J. C. Cardoso, V. Manoharan, A. L. Cristino, N. S. Bhise, W. A. Araujo, P. Zorlutuna, N. E. Vrana, A. M. Ghaemmaghami, M. R. Dokmeci, and A. Khademhosseini. Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 6:024105, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Bertassoni, L. E., M. Cecconi, V. Manoharan, M. Nikkhah, J. Hjortnaes, A. L. Cristino, G. Barabaschi, D. Demarchi, M. R. Dokmeci, Y. Yang, and A. Khademhosseini. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14:2202–2211, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cai, S., H. Xu, Q. Jiang, and Y. Yang. Novel 3D electrospun scaffolds with fibers oriented randomly and evenly in three dimensions to closely mimic the unique architectures of extracellular matrices in soft tissues: fabrication and mechanism study. Langmuir 29:2311–2318, 2013.

    Article  CAS  PubMed  Google Scholar 

  7. Carrier, R. L., M. Rupnick, R. Langer, F. J. Schoen, L. E. Freed, and G. Vunjak-Novakovic. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 8:175–188, 2002.

    Article  CAS  PubMed  Google Scholar 

  8. Centola, M., A. Rainer, C. Spadaccio, S. De Porcellinis, J. A. Genovese, and M. Trombetta. Combining electrospinning and fused deposition modeling for the fabrication of a hybrid vascular graft. Biofabrication 2:014102, 2010.

    Article  CAS  PubMed  Google Scholar 

  9. Chan, T. R., P. J. Stahl, and S. M. Yu. Matrix-Bound VEGF Mimetic Peptides: Design and Endothelial Cell Activation in Collagen Scaffolds. Adv Funct Mater 21:4252–4262, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chang, C. C., E. D. Boland, S. K. Williams, and J. B. Hoying. Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater 98:160–170, 2011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Chang, R., K. Emami, H. Wu, and W. Sun. Biofabrication of a three-dimensional liver micro-organ as an in vitro drug metabolism model. Biofabrication 2:045004, 2010.

    Article  PubMed  CAS  Google Scholar 

  12. Cui, X., and T. Boland. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30:6221–6227, 2009.

    Article  CAS  PubMed  Google Scholar 

  13. Cui, X., T. Boland, D. D. D’Lima, and M. K. Lotz. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat Drug Deliv Formul 6:149–155, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Cui, X., D. Dean, Z. M. Ruggeri, and T. Boland. Cell damage evaluation of thermal inkjet printed Chinese hamster ovary cells. Biotechnol Bioeng 106:963–969, 2010.

    Article  CAS  PubMed  Google Scholar 

  15. Czajka, C. A., A. N. Mehesz, T. C. Trusk, M. J. Yost, and C. J. Drake. Scaffold-free tissue engineering: organization of the tissue cytoskeleton and its effects on tissue shape. Ann Biomed Eng 42:1049–1061, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  16. D’Souza, S. E., M. H. Ginsberg, and E. F. Plow. Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem Sci 16:246–250, 1991.

    Article  PubMed  Google Scholar 

  17. Davis, M. E., J. P. Motion, D. A. Narmoneva, T. Takahashi, D. Hakuno, R. D. Kamm, S. Zhang, and R. T. Lee. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation 111:442–450, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Den Buijs, J. O., D. Dragomir-Daescu, and E. L. Ritman. Cyclic deformation-induced solute transport in tissue scaffolds with computer designed, interconnected, pore networks: experiments and simulations. Ann Biomed Eng 37:1601–1612, 2009.

    Article  Google Scholar 

  19. Dennis, S. G., T. Trusk, D. Richards, J. Jia, Y. Tan, Y. Mei, S. Fann, R. Markwald, and M. Yost. Viability of bioprinted cellular constructs using a three dispenser cartesian printer. J Vis Exp 2015. doi:10.3791/53156.

    PubMed Central  Google Scholar 

  20. Ebrahimkhani, M. R., C. L. Young, D. A. Lauffenburger, L. G. Griffith, and J. T. Borenstein. Approaches to in vitro tissue regeneration with application for human disease modeling and drug development. Drug Discov Today 19:754–762, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fleming, P. A., W. S. Argraves, C. Gentile, A. Neagu, G. Forgacs, and C. J. Drake. Fusion of uniluminal vascular spheroids: a model for assembly of blood vessels. Dev Dyn 239:398–406, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Foty, R. A., and M. S. Steinberg. The differential adhesion hypothesis: a direct evaluation. Dev Biol 278:255–263, 2005.

    Article  CAS  PubMed  Google Scholar 

  23. Gao, G., and X. Cui. Three-dimensional bioprinting in tissue engineering and regenerative medicine. Biotechnol Lett 38:203–211, 2015.

    Article  PubMed  CAS  Google Scholar 

  24. Gao, Q., Y. He, J. Z. Fu, A. Liu, and L. Ma. Coaxial nozzle-assisted 3D bioprinting with built-in microchannels for nutrients delivery. Biomaterials 61:203–215, 2015.

    Article  CAS  PubMed  Google Scholar 

  25. Gentile, C., P. A. Fleming, V. Mironov, K. M. Argraves, W. S. Argraves, and C. J. Drake. VEGF-mediated fusion in the generation of uniluminal vascular spheroids. Dev Dyn 237:2918–2925, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Griffith, L. G., and M. A. Swartz. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7:211–224, 2006.

    Article  CAS  PubMed  Google Scholar 

  27. Guillemot, F., A. Souquet, S. Catros, and B. Guillotin. Laser-assisted cell printing: principle, physical parameters versus cell fate and perspectives in tissue engineering. Nanomedicine (Lond) 5:507–515, 2010.

    Article  Google Scholar 

  28. Guillemot, F., A. Souquet, S. Catros, B. Guillotin, J. Lopez, M. Faucon, B. Pippenger, R. Bareille, M. Remy, S. Bellance, P. Chabassier, J. C. Fricain, and J. Amedee. High-throughput laser printing of cells and biomaterials for tissue engineering. Acta Biomater 6:2494–2500, 2010.

    Article  CAS  PubMed  Google Scholar 

  29. Guillotin, B., A. Souquet, S. Catros, M. Duocastella, B. Pippenger, S. Bellance, R. Bareille, M. Remy, L. Bordenave, J. Amedee, and F. Guillemot. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31:7250–7256, 2010.

    Article  CAS  PubMed  Google Scholar 

  30. Hasan, A., A. Memic, N. Annabi, M. Hossain, A. Paul, M. R. Dokmeci, F. Dehghani, and A. Khademhosseini. Electrospun scaffolds for tissue engineering of vascular grafts. Acta Biomater 10:11–25, 2014.

    Article  CAS  PubMed  Google Scholar 

  31. Hinsbergh, V. W., A. Collen, and P. Koolwijk. Role of fibrin matrix in angiogenesis. Ann NY Acad Sci 936:426–437, 2001.

    Article  PubMed  Google Scholar 

  32. Hinton, T. J., Q. Jallerat, R. N. Palchesko, J. H. Park, M. S. Grodzicki, H. J. Shue, M. H. Ramadan, A. R. Hudson, and A. W. Feinberg. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv 1:e1500758, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Hollister, S. J. Porous scaffold design for tissue engineering. Nat Mater 4:518–524, 2005.

    Article  CAS  PubMed  Google Scholar 

  34. Hu, J., X. Sun, H. Ma, C. Xie, Y. E. Chen, and P. X. Ma. Porous nanofibrous PLLA scaffolds for vascular tissue engineering. Biomaterials 31:7971–7977, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hutmacher, D. W., M. Sittinger, and M. V. Risbud. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends Biotechnol 22:354–362, 2004.

    Article  CAS  PubMed  Google Scholar 

  36. Jakab, K., A. Neagu, V. Mironov, R. R. Markwald, and G. Forgacs. Engineering biological structures of prescribed shape using self-assembling multicellular systems. Proc Natl Acad Sci USA 101:2864–2869, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jakab, K., C. Norotte, B. Damon, F. Marga, A. Neagu, C. L. Besch-Williford, A. Kachurin, K. H. Church, H. Park, V. Mironov, R. Markwald, G. Vunjak-Novakovic, and G. Forgacs. Tissue engineering by self-assembly of cells printed into topologically defined structures. Tissue Eng Part A 14:413–421, 2008.

    Article  CAS  PubMed  Google Scholar 

  38. Jakab, K., C. Norotte, F. Marga, K. Murphy, G. Vunjak-Novakovic, and G. Forgacs. Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2:022001, 2010.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Janmey, P. A., J. P. Winer, and J. W. Weisel. Fibrin gels and their clinical and bioengineering applications. J R Soc Interface 6:1–10, 2009.

    Article  CAS  PubMed  Google Scholar 

  40. Jia, J., D. J. Richards, S. Pollard, Y. Tan, J. Rodriguez, R. P. Visconti, T. C. Trusk, M. J. Yost, H. Yao, R. R. Markwald, and Y. Mei. Engineering alginate as bioink for bioprinting. Acta Biomater 10:4323–4331, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Joshi, V. S., N. Y. Lei, C. M. Walthers, B. Wu, and J. C. Dunn. Macroporosity enhances vascularization of electrospun scaffolds. J Surg Res 183:18–26, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Jungst, T., W. Smolan, K. Schacht, T. Scheibel, and J. Groll. Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev 116:1496–1539, 2015.

    Article  PubMed  CAS  Google Scholar 

  43. Kelm, J. M., V. Djonov, L. M. Ittner, D. Fluri, W. Born, S. P. Hoerstrup, and M. Fussenegger. Design of custom-shaped vascularized tissues using microtissue spheroids as minimal building units. Tissue Eng 12:2151–2160, 2006.

    Article  PubMed  Google Scholar 

  44. Khalil, S., and W. Sun. Bioprinting endothelial cells with alginate for 3D tissue constructs. J Biomech Eng 131:111002, 2009.

    Article  PubMed  Google Scholar 

  45. Khetani, S. R., and S. N. Bhatia. Engineering tissues for in vitro applications. Curr Opin Biotechnol 17:524–531, 2006.

    Article  CAS  PubMed  Google Scholar 

  46. Kolesky, D. B., K. A. Homan, M. A. Skylar-Scott, and J. A. Lewis. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci USA 113:3179–3184, 2016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kolesky, D. B., R. L. Truby, A. S. Gladman, T. A. Busbee, K. A. Homan, and J. A. Lewis. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 26:3124–3130, 2014.

    Article  CAS  PubMed  Google Scholar 

  48. Kumar, A., and B. Starly. Large scale industrialized cell expansion: producing the critical raw material for biofabrication processes. Biofabrication 7:044103, 2015.

    Article  PubMed  Google Scholar 

  49. Laschke, M. W., and M. D. Menger. Vascularization in tissue engineering: angiogenesis versus inosculation. Eur Surg Res 48:85–92, 2012.

    Article  CAS  PubMed  Google Scholar 

  50. Laurens, N., P. Koolwijk, and M. P. de Maat. Fibrin structure and wound healing. J Thromb Haemost 4:932–939, 2006.

    Article  CAS  PubMed  Google Scholar 

  51. Lee, K. Y., and D. J. Mooney. Alginate: properties and biomedical applications. Prog Polym Sci 37:106–126, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lee, M., and H. Y. Kim. Toward nanoscale three-dimensional printing: nanowalls built of electrospun nanofibers. Langmuir 30:1210–1214, 2014.

    Article  CAS  PubMed  Google Scholar 

  53. Lee, M., and B. M. Wu. Recent advances in 3D printing of tissue engineering scaffolds. Methods Mol Biol 868:257–267, 2012.

    Article  CAS  PubMed  Google Scholar 

  54. Lee, V. K., D. Y. Kim, H. Ngo, Y. Lee, L. Seo, S. S. Yoo, P. A. Vincent, and G. Dai. Creating perfused functional vascular channels using 3D bio-printing technology. Biomaterials 35:8092–8102, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lee, V. K., A. M. Lanzi, N. Haygan, S. S. Yoo, P. A. Vincent, and G. Dai. Generation of multi-scale vascular network system within 3D hydrogel using 3D bio-printing technology. Cell Mol Bioeng 7:460–472, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lee, W., V. Lee, S. Polio, P. Keegan, J. H. Lee, K. Fischer, J. K. Park, and S. S. Yoo. On-demand three-dimensional freeform fabrication of multi-layered hydrogel scaffold with fluidic channels. Biotechnol Bioeng 105:1178–1186, 2010.

    CAS  PubMed  Google Scholar 

  57. Lee, Y.-B., S. Polio, W. Lee, G. Dai, L. Menon, R. S. Carroll, and S.-S. Yoo. Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture. Exp Neurol 223:645–652, 2010.

    Article  CAS  PubMed  Google Scholar 

  58. Leslie-Barbick, J. E., J. E. Saik, D. J. Gould, M. E. Dickinson, and J. L. West. The promotion of microvasculature formation in poly(ethylene glycol) diacrylate hydrogels by an immobilized VEGF-mimetic peptide. Biomaterials 32:5782–5789, 2011.

    Article  CAS  PubMed  Google Scholar 

  59. Li, Z., X. Guo, and J. Guan. An oxygen release system to augment cardiac progenitor cell survival and differentiation under hypoxic condition. Biomaterials 33:5914–5923, 2012.

    Article  CAS  PubMed  Google Scholar 

  60. Lin, C. Y., Y. R. Wang, C. W. Lin, S. W. Wang, H. W. Chien, N. C. Cheng, W. B. Tsai, and J. Yu. Peptide-modified zwitterionic porous hydrogels for endothelial cell and vascular engineering. Biores Open Access 3:297–310, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lin, Y. D., M. Y. Chang, B. Cheng, Y. W. Liu, L. C. Lin, J. H. Chen, and P. C. Hsieh. Injection of Peptide nanogels preserves postinfarct diastolic function and prolongs efficacy of cell therapy in pigs. Tissue Eng Part A 21:1662–1671, 2015.

    Article  CAS  PubMed  Google Scholar 

  62. Lin, Y. D., C. Y. Luo, Y. N. Hu, M. L. Yeh, Y. C. Hsueh, M. Y. Chang, D. C. Tsai, J. N. Wang, M. J. Tang, E. I. Wei, M. L. Springer, and P. C. Hsieh. Instructive nanofiber scaffolds with VEGF create a microenvironment for arteriogenesis and cardiac repair. Sci Transl Med 4:146ra109, 2012.

    PubMed  Google Scholar 

  63. Lin, Y. D., M. L. Yeh, Y. J. Yang, D. C. Tsai, T. Y. Chu, Y. Y. Shih, M. Y. Chang, Y. W. Liu, A. C. Tang, T. Y. Chen, C. Y. Luo, K. C. Chang, J. H. Chen, H. L. Wu, T. K. Hung, and P. C. Hsieh. Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation 122:S132–141, 2010.

    Article  CAS  PubMed  Google Scholar 

  64. Loo, Y., A. Lakshmanan, M. Ni, L. L. Toh, S. Wang, and C. A. Hauser. Peptide bioink: self-assembling nanofibrous scaffolds for three-dimensional organotypic cultures. Nano Lett 15:6919–6925, 2015.

    Article  CAS  PubMed  Google Scholar 

  65. Lovett, M., K. Lee, A. Edwards, and D. L. Kaplan. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev 15:353–370, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Mace, J., A. Wheelton, W. S. Khan, and S. Anand. The role of bioreactors in ligament and tendon tissue engineering. Curr Stem Cell Res Ther 11:35–40, 2016.

    Article  CAS  PubMed  Google Scholar 

  67. Maidhof, R., N. Tandon, E. J. Lee, J. Luo, Y. Duan, K. Yeager, E. Konofagou, and G. Vunjak-Novakovic. Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue. J Tissue Eng Regen Med 6:e12–23, 2012.

    Article  PubMed  Google Scholar 

  68. Malda, J., T. J. Klein, and Z. Upton. The roles of hypoxia in the in vitro engineering of tissues. Tissue Eng 13:2153–2162, 2007.

    Article  CAS  PubMed  Google Scholar 

  69. Mandrycky, C., Z. Wang, K. Kim, and D. H. Kim. 3D bioprinting for engineering complex tissues. Biotechnol Adv 2015. doi:10.1016/j.biotechadv.2015.12.011.

    PubMed  Google Scholar 

  70. Marga, F., K. Jakab, C. Khatiwala, B. Shepherd, S. Dorfman, B. Hubbard, S. Colbert, and F. Gabor. Toward engineering functional organ modules by additive manufacturing. Biofabrication 4:022001, 2012.

    Article  PubMed  Google Scholar 

  71. Martin, Y., and P. Vermette. Bioreactors for tissue mass culture: design, characterization, and recent advances. Biomaterials 26:7481–7503, 2005.

    Article  CAS  PubMed  Google Scholar 

  72. Miller, J. S., K. R. Stevens, M. T. Yang, B. M. Baker, D. H. Nguyen, D. M. Cohen, E. Toro, A. A. Chen, P. A. Galie, X. Yu, R. Chaturvedi, S. N. Bhatia, and C. S. Chen. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11:768–774, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mironov, V., V. Kasyanov, and R. R. Markwald. Organ printing: from bioprinter to organ biofabrication line. Curr Opin Biotechnol 22:667–673, 2011.

    Article  CAS  PubMed  Google Scholar 

  74. Mironov, V., R. P. Visconti, V. Kasyanov, G. Forgacs, C. J. Drake, and R. R. Markwald. Organ printing: tissue spheroids as building blocks. Biomaterials 30:2164–2174, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Mun, C. H., Y. Jung, S. H. Kim, H. C. Kim, and S. H. Kim. Effects of pulsatile bioreactor culture on vascular smooth muscle cells seeded on electrospun poly (lactide-co-epsilon-caprolactone) scaffold. Artif Organs 37:E168–178, 2013.

    Article  CAS  PubMed  Google Scholar 

  76. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat Biotechnol 32:773–785, 2014.

    Article  CAS  PubMed  Google Scholar 

  77. Nakamura, M., S. Iwanaga, C. Henmi, K. Arai, and Y. Nishiyama. Biomatrices and biomaterials for future developments of bioprinting and biofabrication. Biofabrication 2:014110, 2010.

    Article  CAS  PubMed  Google Scholar 

  78. Nakamura, M., Y. Nishiyama, C. Henmi, S. Iwanaga, H. Nakagawa, K. Yamaguchi, K. Akita, S. Mochizuki, and K. Takiura. Ink jet three-dimensional digital fabrication for biological tissue manufacturing: analysis of alginate microgel beads produced by ink jet droplets for three dimensional tissue fabrication. J Imaging Sci Technol 52:60201, 2008.

    Article  CAS  Google Scholar 

  79. Narmoneva, D. A., O. Oni, A. L. Sieminski, S. Zhang, J. P. Gertler, R. D. Kamm, and R. T. Lee. Self-assembling short oligopeptides and the promotion of angiogenesis. Biomaterials 26:4837–4846, 2005.

    Article  CAS  PubMed  Google Scholar 

  80. Nguyen, D. H., S. C. Stapleton, M. T. Yang, S. S. Cha, C. K. Choi, P. A. Galie, and C. S. Chen. Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro. Proc Natl Acad Sci USA 110:6712–6717, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Nicosia, R. F., and A. Ottinetti. Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Laboratory investigation; a journal of technical methods and pathology 63:115–122, 1990.

    CAS  PubMed  Google Scholar 

  82. Nishiyama, Y., M. Nakamura, C. Henmi, K. Yamaguchi, S. Mochizuki, H. Nakagawa, and K. Takiura. Development of a three-dimensional bioprinter: construction of cell supporting structures using hydrogel and state-of-the-art inkjet technology. J Biomech Eng 131:035001, 2009.

    Article  PubMed  Google Scholar 

  83. Norotte, C., F. S. Marga, L. E. Niklason, and G. Forgacs. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Novosel, E. C., C. Kleinhans, and P. J. Kluger. Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63:300–311, 2011.

    Article  CAS  PubMed  Google Scholar 

  85. Oh, S. H., C. L. Ward, A. Atala, J. J. Yoo, and B. S. Harrison. Oxygen generating scaffolds for enhancing engineered tissue survival. Biomaterials 30:757–762, 2009.

    Article  CAS  PubMed  Google Scholar 

  86. Otrock, Z. K., R. A. Mahfouz, J. A. Makarem, and A. I. Shamseddine. Understanding the biology of angiogenesis: review of the most important molecular mechanisms. Blood Cells Mol Dis 39:212–220, 2007.

    Article  CAS  PubMed  Google Scholar 

  87. Ozbolat, I. T. Bioprinting scale-up tissue and organ constructs for transplantation. Trends Biotechnol 33:395–400, 2015.

    Article  CAS  PubMed  Google Scholar 

  88. Park, H., B. L. Larson, M. D. Guillemette, S. R. Jain, C. Hua, G. C. Engelmayr, Jr, and L. E. Freed. The significance of pore microarchitecture in a multi-layered elastomeric scaffold for contractile cardiac muscle constructs. Biomaterials 32:1856–1864, 2011.

    Article  CAS  PubMed  Google Scholar 

  89. Pataky, K., T. Braschler, A. Negro, P. Renaud, M. P. Lutolf, and J. Brugger. Microdrop printing of hydrogel bioinks into 3D tissue-like geometries. Adv Mater 24:391–396, 2012.

    Article  CAS  PubMed  Google Scholar 

  90. Pathi, P., T. Ma, and B. R. Locke. Role of nutrient supply on cell growth in bioreactor design for tissue engineering of hematopoietic cells. Biotechnol Bioeng 89:743–758, 2005.

    Article  CAS  PubMed  Google Scholar 

  91. Pati, F., J. Jang, D. H. Ha, S. Won Kim, J. W. Rhie, J. H. Shim, D. H. Kim, and D. W. Cho. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Paulsen, S. J., and J. S. Miller. Tissue vascularization through 3D printing: will technology bring us flow? Dev Dyn 244:629–640, 2015.

    Article  CAS  PubMed  Google Scholar 

  93. Phelps, E. A., and A. J. Garcia. Engineering more than a cell: vascularization strategies in tissue engineering. Curr Opin Biotechnol 21:704–709, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Radisic, M., J. Malda, E. Epping, W. Geng, R. Langer, and G. Vunjak-Novakovic. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 93:332–343, 2006.

    Article  CAS  PubMed  Google Scholar 

  95. Radisic, M., H. Park, F. Chen, J. E. Salazar-Lazzaro, Y. Wang, R. Dennis, R. Langer, L. E. Freed, and G. Vunjak-Novakovic. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12:2077–2091, 2006.

    Article  CAS  PubMed  Google Scholar 

  96. Raimondi, M. T. Engineered tissue as a model to study cell and tissue function from a biophysical perspective. Curr Drug Discov Technol 3:245–268, 2006.

    Article  CAS  PubMed  Google Scholar 

  97. Riess, J. G. Perfluorocarbon-based oxygen delivery. Artif Cells Blood Substit Immobil Biotechnol 34:567–580, 2006.

    Article  CAS  PubMed  Google Scholar 

  98. Rioja, A. Y., R. T. Annamalai, S. Paris, A. J. Putnam, and J. P. Stegemann. Endothelial sprouting and network formation in collagen- and fibrin-based modular microbeads. Acta Biomater 29:33–41, 2016.

    Article  CAS  PubMed  Google Scholar 

  99. Rouwkema, J., B. Koopman, C. Blitterswijk, W. Dhert, and J. Malda. Supply of nutrients to cells in engineered tissues. Biotechnol Genet Eng Rev 26:163–178, 2010.

    Article  CAS  PubMed  Google Scholar 

  100. Rouwkema, J., N. C. Rivron, and C. A. van Blitterswijk. Vascularization in tissue engineering. Trends Biotechnol 26:434–441, 2008.

    Article  CAS  PubMed  Google Scholar 

  101. Rutz, A. L., K. E. Hyland, A. E. Jakus, W. R. Burghardt, and R. N. Shah. A multimaterial bioink method for 3D printing tunable, cell-compatible hydrogels. Adv Mater 27:1607–1614, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Schultz, G. S., and A. Wysocki. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen 17:153–162, 2009.

    Article  PubMed  Google Scholar 

  103. Schuurman, W., P. A. Levett, M. W. Pot, P. R. van Weeren, W. J. Dhert, D. W. Hutmacher, F. P. Melchels, T. J. Klein, and J. Malda. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol Biosci 13:551–561, 2013.

    Article  CAS  PubMed  Google Scholar 

  104. Shaikh, F. M., A. Callanan, E. G. Kavanagh, P. E. Burke, P. A. Grace, and T. M. McGloughlin. Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs 188:333–346, 2008.

    Article  CAS  PubMed  Google Scholar 

  105. Skardal, A., J. Zhang, L. McCoard, X. Xu, S. Oottamasathien, and G. D. Prestwich. Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Eng Part A 16:2675–2685, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  107. Sooppan, R., S. J. Paulsen, J. Han, A. H. Ta, P. Dinh, A. C. Gaffey, C. Venkataraman, A. Trubelja, G. Hung, J. S. Miller, and P. Atluri. In vivo anastomosis and perfusion of a three-dimensionally-printed construct containing microchannel networks. Tissue Eng Part C Methods 22:1–7, 2016.

    Article  CAS  PubMed  Google Scholar 

  108. Sosnik, A., D. Cohn, J. San Roman, and G. A. Abraham. Crosslinkable PEO-PPO-PEO-based reverse thermo-responsive gels as potentially injectable materials. J Biomater Sci Polym Ed 14:227–239, 2003.

    Article  CAS  PubMed  Google Scholar 

  109. Tan, Q., A. M. El-Badry, C. Contaldo, R. Steiner, S. Hillinger, M. Welti, M. Hilbe, D. R. Spahn, R. Jaussi, G. Higuera, C. A. van Blitterswijk, Q. Luo, and W. Weder. The effect of perfluorocarbon-based artificial oxygen carriers on tissue-engineered trachea. Tissue Eng Part A 15:2471–2480, 2009.

    Article  CAS  PubMed  Google Scholar 

  110. Tan, Y., D. J. Richards, T. C. Trusk, R. P. Visconti, M. J. Yost, M. S. Kindy, C. J. Drake, W. S. Argraves, R. R. Markwald, and Y. Mei. 3D printing facilitated scaffold-free tissue unit fabrication. Biofabrication 6:024111, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Tibbitt, M. W., C. B. Rodell, J. A. Burdick, and K. S. Anseth. Progress in material design for biomedical applications. Proc Natl Acad Sci USA 112:14444–14451, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Tumbleston, J. R., D. Shirvanyants, N. Ermoshkin, R. Janusziewicz, A. R. Johnson, D. Kelly, K. Chen, R. Pinschmidt, J. P. Rolland, A. Ermoshkin, E. T. Samulski, and J. M. DeSimone. Additive manufacturing. Continuous liquid interface production of 3D objects. Science 347:1349–1352, 2015.

    Article  CAS  PubMed  Google Scholar 

  113. Van Den Bulcke, A. I., B. Bogdanov, N. De Rooze, E. H. Schacht, M. Cornelissen, and H. Berghmans. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules 1:31–38, 2000.

    Article  CAS  Google Scholar 

  114. Visconti, R. P., V. Kasyanov, C. Gentile, J. Zhang, R. R. Markwald, and V. Mironov. Towards organ printing: engineering an intra-organ branched vascular tree. Expert Opin Biol Ther 10:409–420, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Visser, J., P. A. Levett, N. C. te Moller, J. Besems, K. W. Boere, M. H. van Rijen, J. C. de Grauw, W. J. Dhert, P. R. van Weeren, and J. Malda. Crosslinkable hydrogels derived from cartilage, meniscus, and tendon tissue. Tissue Eng Part A 21:1195–1206, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Visser, J., F. P. Melchels, J. E. Jeon, E. M. van Bussel, L. S. Kimpton, H. M. Byrne, W. J. Dhert, P. D. Dalton, D. W. Hutmacher, and J. Malda. Reinforcement of hydrogels using three-dimensionally printed microfibres. Nat Commun 6:6933, 2015.

    Article  CAS  PubMed  Google Scholar 

  117. Visser, J., B. Peters, T. J. Burger, J. Boomstra, W. J. Dhert, F. P. Melchels, and J. Malda. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 5:035007, 2013.

    Article  PubMed  CAS  Google Scholar 

  118. Walthers, C. M., A. K. Nazemi, S. L. Patel, B. M. Wu, and J. C. Dunn. The effect of scaffold macroporosity on angiogenesis and cell survival in tissue-engineered smooth muscle. Biomaterials 35:5129–5137, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Wang, L., M. Zhao, S. Li, U. J. Erasquin, H. Wang, L. Ren, C. Chen, Y. Wang, and C. Cai. “Click” immobilization of a VEGF-mimetic peptide on decellularized endothelial extracellular matrix to enhance angiogenesis. ACS Appl Mater Interfaces 6:8401–8406, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Welti, J., S. Loges, S. Dimmeler, and P. Carmeliet. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Investig 123:3190–3200, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Wilgus, T. A. Growth factor-extracellular matrix interactions regulate wound repair. Adv Wound Care (New Rochelle) 1:249–254, 2012.

    Article  PubMed Central  Google Scholar 

  122. Woodfield, T. B., L. Moroni, and J. Malda. Combinatorial approaches to controlling cell behaviour and tissue formation in 3D via rapid-prototyping and smart scaffold design. Comb Chem High Throughput Screen 12:562–579, 2009.

    Article  CAS  PubMed  Google Scholar 

  123. Wu, P. K., and B. R. Ringeisen. Development of human umbilical vein endothelial cell (HUVEC) and human umbilical vein smooth muscle cell (HUVSMC) branch/stem structures on hydrogel layers via biological laser printing (BioLP). Biofabrication 2:014111, 2010.

    Article  CAS  PubMed  Google Scholar 

  124. Wu, W., A. DeConinck, and J. A. Lewis. Omnidirectional printing of 3D microvascular networks. Adv Mater 23:H178–183, 2011.

    Article  CAS  PubMed  Google Scholar 

  125. Xu, T., C. Baicu, M. Aho, M. Zile, and T. Boland. Fabrication and characterization of bio-engineered cardiac pseudo tissues. Biofabrication 1:035001, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Xu, T., K. W. Binder, M. Z. Albanna, D. Dice, W. Zhao, J. J. Yoo, and A. Atala. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication 5:015001, 2013.

    Article  PubMed  CAS  Google Scholar 

  127. Xu, T., J. Jin, C. Gregory, J. J. Hickman, and T. Boland. Inkjet printing of viable mammalian cells. Biomaterials 26:93–99, 2005.

    Article  PubMed  CAS  Google Scholar 

  128. Yeong, W. Y., C. K. Chua, K. F. Leong, and M. Chandrasekaran. Rapid prototyping in tissue engineering: challenges and potential. Trends Biotechnol 22:643–652, 2004.

    Article  CAS  PubMed  Google Scholar 

  129. Zhang, Y., Y. Yu, H. Chen, and I. T. Ozbolat. Characterization of printable cellular micro-fluidic channels for tissue engineering. Biofabrication 5:025004, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Zhao, L., V. K. Lee, S.-S. Yoo, G. Dai, and X. Intes. The integration of 3-D cell printing and mesoscopic fluorescence molecular tomography of vascular constructs within thick hydrogel scaffolds. Biomaterials 33:5325–5332, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Zheng, Y., J. Chen, M. Craven, N. W. Choi, S. Totorica, A. Diaz-Santana, P. Kermani, B. Hempstead, C. Fischbach-Teschl, and J. A. López. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci USA 109:9342–9347, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The work is supported by the National Institutes of Health (8P20 GM103444, U54 GM104941), the startup funds from Clemson University, the National Science Foundation (NSF - EPS-0903795), the NIH Cardiovascular Training Grant (T32 HL007260), and by NIH-NIGMS P30 GM103342 to the South Carolina COBRE for Developmentally Based Cardiovascular Diseases.

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Associate Editor Jos Malda oversaw the review of this article.

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Richards, D., Jia, J., Yost, M. et al. 3D Bioprinting for Vascularized Tissue Fabrication. Ann Biomed Eng 45, 132–147 (2017). https://doi.org/10.1007/s10439-016-1653-z

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