Biomaterials for Integration with 3-D Bioprinting

Annals of Biomedical Engineering

Volumn 43, Issue 3, 2015, Pages 730-746

  Skardal, Aleksander ^a   Atala, Anthony ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Biocompatibility; Biofabrication; Bioink; Biomaterials; Bioprinting; Cells; Hydrogel; Stability; Viability

Indexed keywords

BIOCOMPATIBILITY; BIOLOGICAL MATERIALS; BIOMATERIALS; CELLS; CONVERGENCE OF NUMERICAL METHODS; DIAGNOSIS; HISTOLOGY; HYDROGELS; MEDICINE; MOBILE SECURITY; TISSUE;

BIOFABRICATION; BIOINK; BIOPRINTING; CELLULAR COMPONENTS; LASER INDUCED FORWARD TRANSFER; REGENERATIVE MEDICINE; SYNTHETIC POLYMERS; VIABILITY;

TISSUE ENGINEERING;

ALGINIC ACID; BIOMATERIAL; COLLAGEN; GELATIN; HYALURONIC ACID;

ARTICLE; BIOCOMPATIBILITY; BIOPRINTING; CELL ADHESION; CELL VIABILITY; CHEMICAL MODIFICATION; COMPRESSION; CROSS LINKING; GEL; HIGH TEMPERATURE; HYDROGEL; POLYMERIZATION; PRIORITY JOURNAL; SCALE UP; SHEAR STRESS; TEMPERATURE; TEMPERATURE SENSITIVITY; TISSUE ENGINEERING; ULTRAVIOLET IRRADIATION; YOUNG MODULUS; ANIMAL; HUMAN; THREE DIMENSIONAL PRINTING;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOPRINTING; HUMANS; PRINTING, THREE-DIMENSIONAL;

EID: 84925745420     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-014-1207-1     Document Type: Article

References (90)

1. Ahmed, T. A., E. V. Dare, and M. Hincke. Fibrin: a versatile scaffold for tissue engineering applications. Tissue Eng. Part B Rev. 14:199–215, 2008.
2. Allison, D. D., and K. J. Grande-Allen. Review. Hyaluronan: a powerful tissue engineering tool. Tissue Eng. 12:2131–2140, 2006.
3. Balzar, M., F. A. Prins, H. A. Bakker, G. J. Fleuren, S. O. Warnaar, and S. V. Litvinov. The structural analysis of adhesions mediated by Ep-CAM. Exp. Cell Res. 246:108–121, 1999.
4. Barron, J. A., B. R. Ringeisen, H. Kim, B. J. Spargo, and D. B. Chrisey. Application of laser printing to mammalian cells. Thin Solid Films. 453:383–387, 2004.
5. 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.
6. 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.
7. Billiet, T., M. Vandenhaute, J. Schelfhout, S. Van Vlierberghe, and P. Dubruel. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials. 33:6020–6041, 2012.
8. Bohandy, J., B. Kim, and F. Adrian. Metal deposition from a supported metal film using an excimer laser. J. Appl. Phys. 60:1538, 1986.
9. Boland, T., V. Mironov, A. Gutowska, E. A. Roth, and R. R. Markwald. Cell and organ printing 2: fusion of cell aggregates in three-dimensional gels. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 272:497–502, 2003.
10. Boland, T., T. Xu, B. Damon, and X. Cui. Application of inkjet printing to tissue engineering. Biotechnol. J. 1:910–917, 2006.
11. Brodkey, B. S. Non-Newtonian Phenomena. The Phenomena of Fluid Motions. Reading: Addison-Welsley, 1967.
12. Catros, S., J. C. Fricain, B. Guillotin, B. Pippenger, R. Bareille, M. Remy, E. Lebraud, B. Desbat, J. Amedee, and F. Guillemot. Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication. 3:025001, 2011.
13. Chrisey, D. B. Materials processing: the power of direct writing. Science. 289:879–881, 2000.
14. Cohen, J., K. L. Zaleski, G. Nourissat, T. P. Julien, M. A. Randolph, and M. J. Yaremchuk. Survival of porcine mesenchymal stem cells over the alginate recovered cellular method. J. Biomed. Mater. Res. A. 96:93–99, 2011.
15. Colina, M., P. Serra, J. M. Fernandez-Pradas, L. Sevilla, and J. L. Morenza. DNA deposition through laser induced forward transfer. Biosens. Bioelectron. 20:1638–1642, 2005.
16. Dainiak, M. B., I. U. Allan, I. N. Savina, L. Cornelio, E. S. James, S. L. James, S. V. Mikhalovsky, H. Jungvid, and I. Y. Galaev. Gelatin-fibrinogen cryogel dermal matrices for wound repair: preparation, optimisation and in vitro study. Biomaterials. 31:67–76, 2010.
17. Derby, B. Printing and prototyping of tissues and scaffolds. Science. 338:921–926, 2012.
18. Dinca, V., E. Kasotakis, J. Catherine, A. Mourka, A. Ranella, A. Ovsianikov, B. N. Chichkov, M. Farsari, A. Mitraki, and C. Fotakis. Directed three-dimensional patterning of self-assembled peptide fibrils. Nano Lett. 8:538–543, 2008.
19. du Moon, G., G. Christ, J. D. Stitzel, A. Atala, and J. J. Yoo. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng. Part A. 14:473–482, 2008.
20. Dubsky, M., S. Kubinova, J. Sirc, L. Voska, R. Zajicek, A. Zajicova, P. Lesny, A. Jirkovska, J. Michalek, M. Munzarova, V. Holan, and E. Sykova. Nanofibers prepared by needleless electrospinning technology as scaffolds for wound healing. J. Mater. Sci. Mater. Med. 23:931–941, 2012.
21. Fedorovich, N. E., J. Alblas, J. R. de Wijn, W. E. Hennink, A. J. Verbout, and W. J. Dhert. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng. 13:1905–1925, 2007.
22. Ferris, C. J., K. G. Gilmore, and G. G. Wallace. Biofabrication: an overview of the approaches used for printing of living cells. Appl. Microbiol. Biotechnol. 97:4243–4258, 2013.
23. 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.
24. Galus, R., M. Antiszko, and P. Wlodarski. Clinical applications of hyaluronic acid. Pol. Merkur Lekarski. 20:606–608, 2006.
25. Goldstein, A. S., and G. Christ. Functional tissue engineering requires bioreactor strategies. Tissue Eng. Part A. 15:739–740, 2009.
26. Gou, M., X. Qu, W. Zhu, M. Xiang, J. Yang, K. Zhang, Y. Wei, and S. Chen. Bio-inspired detoxification using 3D-printed hydrogel nanocomposites. Nat. Commun. 5:3774, 2014.
27. Gruene, M., A. Deiwick, L. Koch, S. Schlie, C. Unger, N. Hofmann, I. Bernemann, B. Glasmacher, and B. Chichkov. Laser printing of stem cells for biofabrication of scaffold-free autologous grafts. Tissue Eng. Part C 17:79–87, 2010.
28. Guillotin, B., and F. Guillemot. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 29:183–190, 2011.
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.
30. Hahn, M. S., M. K. McHale, E. Wang, R. H. Schmedlen, and J. L. West. Physiologic pulsatile flow bioreactor conditioning of poly(ethylene glycol)-based tissue engineered vascular grafts. Ann. Biomed. Eng. 35:190–200, 2007.
31. Hesse, E., T. E. Hefferan, J. E. Tarara, C. Haasper, R. Meller, C. Krettek, L. Lu, and M. J. Yaszemski. Collagen type I hydrogel allows migration, proliferation, and osteogenic differentiation of rat bone marrow stromal cells. J. Biomed. Mater. Res. A. 94:442–449, 2010.
32. Hopp, B., T. Smausz, N. Kresz, N. Barna, Z. Bor, L. Kolozsvari, D. B. Chrisey, A. Szabo, and A. Nogradi. Survival and proliferative ability of various living cell types after laser-induced forward transfer. Tissue Eng. 11:1817–1823, 2005.
33. Howarth, A. G., and B. R. Stevenson. Molecular environment of ZO-1 in epithelial and non-epithelial cells. Cell Motil. Cytoskelet. 31:323–332, 1995.
34. Hribar, K. C., P. Soman, J. Warner, P. Chung, and S. Chen. Light-assisted direct-write of 3D functional biomaterials. Lab. Chip. 14:268–275, 2014.
35. Iwami, K., T. Noda, K. Ishida, K. Morishima, M. Nakamura, and N. Umeda. Bio rapid prototyping by extruding/aspirating/refilling thermoreversible hydrogel. Biofabrication. 2:014108, 2010.
36. Jakab, K., B. Damon, F. Marga, O. Doaga, V. Mironov, I. Kosztin, R. Markwald, and G. Forgacs. Relating cell and tissue mechanics: implications and applications. Dev. Dyn. 237:2438–2449, 2008.
37. 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.
38. 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.
39. 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.
40. Kanda, N., N. Morimoto, A. A. Ayvazyan, S. Takemoto, K. Kawai, Y. Nakamura, Y. Sakamoto, T. Taira, and S. Suzuki. Evaluation of a novel collagen-gelatin scaffold for achieving the sustained release of basic fibroblast growth factor in a diabetic mouse model. J. Tissue Eng. Regen. Med. 8:29–40, 2014.
41. Kirker, K. R., Y. Luo, S. E. Morris, J. Shelby, and G. D. Prestwich. Glycosaminoglycan hydrogels as supplemental wound dressings for donor sites. J. Burn. Care Rehabil. 25:276–286, 2004.
42. Knudson, C. B., and W. Knudson. Cartilage proteoglycans. Semin. Cell Dev. Biol. 12:69–78, 2001.
43. Koch, L., S. Kuhn, H. Sorg, M. Gruene, S. Schlie, R. Gaebel, B. Polchow, K. Reimers, S. Stoelting, N. Ma, P. M. Vogt, G. Steinhoff, and B. Chichkov. Laser printing of skin cells and human stem cells. Tissue Eng. Part C 16:847–854, 2010.
44. Lee, S. J., J. Liu, S. H. Oh, S. Soker, A. Atala, and J. J. Yoo. Development of a composite vascular scaffolding system that withstands physiological vascular conditions. Biomaterials. 29:2891–2898, 2008.
45. Li, C., P. Chen, Y. Shao, X. Zhou, Y. Wu, Z. Yang, Z. Li, T. Weil, and D. Liu. A writable polypeptide-DNA hydrogel with rationally designed multi-modification sites. Small, 2014. doi:10.1002/smll.201401906.
46. Li, J., X. Li, X. Ni, X. Wang, H. Li, and K. W. Leong. Self-assembled supramolecular hydrogels formed by biodegradable PEO-PHB-PEO triblock copolymers and alpha-cyclodextrin for controlled drug delivery. Biomaterials. 27:4132–4140, 2006.
47. Lin, H., D. Zhang, P. G. Alexander, G. Yang, J. Tan, A. W. Cheng, and R. S. Tuan. Application of visible light-based projection stereolithography for live cell-scaffold fabrication with designed architecture. Biomaterials. 34:331–339, 2013.
48. Liu, Y., X. Z. Shu, and G. D. Prestwich. Tumor engineering: orthotopic cancer models in mice using cell-loaded, injectable, cross-linked hyaluronan-derived hydrogels. Tissue Eng. 13:1091–1101, 2007.
49. Machingal, M. A., B. T. Corona, T. J. Walters, V. Kesireddy, C. N. Koval, A. Dannahower, W. Zhao, J. J. Yoo, and G. J. Christ. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng. Part A. 17:2291–2303, 2011.
50. 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.
51. Matsuura, K., R. Utoh, K. Nagase, and T. Okano. Cell sheet approach for tissue engineering and regenerative medicine. J. Control Release. 190C:228–239, 2014.
52. Miki, D., K. Dastgheib, T. Kim, A. Pfister-Serres, K. A. Smeds, M. Inoue, D. L. Hatchell, and M. W. Grinstaff. A photopolymerized sealant for corneal lacerations. Cornea. 21:393–399, 2002.
53. Mironov, V., T. Boland, T. Trusk, G. Forgacs, and R. R. Markwald. Organ printing: computer-aided jet-based 3D tissue engineering. Trends Biotechnol. 21:157–161, 2003.
54. Mironov, V., V. Kasyanov, C. Drake, and R. R. Markwald. Organ printing: promises and challenges. Regen. Med. 3:93–103, 2008.
55. Mironov, V., V. Kasyanov, K. McAllister, S. Oliver, J. Sistino, and R. Markwald. Perfusion bioreactor for vascular tissue engineering with capacities for longitudinal stretch. J. Craniofac. Surg. 14:340–347, 2003.
56. Mironov, V., G. Prestwich, and G. Forgacs. Bioprinting living structures. J. Mater. Chem. 17:2054–2060, 2007.
57. Mironov, V., N. Reis, and B. Derby. Review: bioprinting: a beginning. Tissue Eng. 12:631–634, 2006.
58. 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.
59. Moon, S., S. K. Hasan, Y. S. Song, F. Xu, H. O. Keles, F. Manzur, S. Mikkilineni, J. W. Hong, J. Nagatomi, E. Haeggstrom, A. Khademhosseini, and U. Demirci. Layer by layer three-dimensional tissue epitaxy by cell-laden hydrogel droplets. Tissue Eng. Part C Methods. 16:157–166, 2010.
60. Muller, M., J. Becher, M. Schnabelrauch, and M. Zenobi-Wong. Printing thermoresponsive reverse molds for the creation of patterned two-component hydrogels for 3D cell culture. J. Vis. Exp. 77:e50632, 2013.
61. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32:773–785, 2014.
62. Murphy, S. V., A. Skardal, and A. Atala. Evaluation of hydrogels for bio-printing applications. J. Biomed. Mater. Res. A. 101:272–284, 2013.
63. Nair, K., M. Gandhi, S. Khalil, K. C. Yan, M. Marcolongo, K. Barbee, and W. Sun. Characterization of cell viability during bioprinting processes. Biotechnol. J. 4:1168–1177, 2009.
64. 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.
65. Norotte, C., F. S. Marga, L. E. Niklason, and G. Forgacs. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials. 30:5910–5917, 2009.
66. Opara, E. C., S. H. Mirmalek-Sani, O. Khanna, M. L. Moya, and E. M. Brey. Design of a bioartificial pancreas(+). J. Investig. Med. 58:831–837, 2010.
67. Parisi-Amon, A., W. Mulyasasmita, C. Chung, and S. C. Heilshorn. Protein-engineered injectable hydrogel to improve retention of transplanted adipose-derived stem cells. Adv. Healthc. Mater. 2:428–432, 2013.
68. Pescosolido, L., W. Schuurman, J. Malda, P. Matricardi, F. Alhaique, T. Coviello, P. R. van Weeren, W. J. Dhert, W. E. Hennink, and T. Vermonden. Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting. Biomacromolecules. 12:1831–1838, 2011.
69. Prestwich, G. D. Evaluating drug efficacy and toxicology in three dimensions: using synthetic extracellular matrices in drug discovery. Acc. Chem. Res. 41:139–148, 2008.
70. Prestwich, G. D., and J. W. Kuo. Chemically-modified HA for therapy and regenerative medicine. Curr. Pharm. Biotechnol. 9:242–245, 2008.
71. Rashid, S. T., B. Fuller, G. Hamilton, and A. M. Seifalian. Tissue engineering of a hybrid bypass graft for coronary and lower limb bypass surgery. FASEB J. 22:2084–2089, 2008.
72. Roth, E. A., T. Xu, M. Das, C. Gregory, J. J. Hickman, and T. Boland. Inkjet printing for high-throughput cell patterning. Biomaterials. 25:3707–3715, 2004.
73. Santos, E., J. Zarate, G. Orive, R. M. Hernandez, and J. L. Pedraz. Biomaterials in cell microencapsulation. Adv. Exp. Med. Biol. 670:5–21, 2010.
74. Scanlon, C. S., E. A. Van Tubergen, R. C. Inglehart, and N. J. D’Silva. Biomarkers of epithelial-mesenchymal transition in squamous cell carcinoma. J. Dent. Res. 92:114–121, 2013.
75. Schiavinato, A., M. Finesso, R. Cortivo, and G. Abatangelo. Comparison of the effects of intra-articular injections of Hyaluronan and its chemically cross-linked derivative (Hylan G-F20) in normal rabbit knee joints. Clin. Exp. Rheumatol. 20:445–454, 2002.
76. Skardal, A., D. Mack, E. Kapetanovic, A. Atala, J. D. Jackson, J. J. Yoo, and S. Soker. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl. Med. 1:792–802, 2012.
77. Skardal, A., L. Smith, S. Bharadwaj, A. Atala, S. Soker, and Y. Zhang. Tissue specific synthetic ECM hydrogels for 3-D in vitro maintenance of hepatocyte function. Biomaterials. 33:4565–4575, 2012.
78. Skardal, A., J. Zhang, L. McCoard, S. Oottamasathien, and G. D. Prestwich. Dynamically crosslinked gold nanoparticle—hyaluronan hydrogels. Adv. Mater. 22:4736–4740, 2010.
79. 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.
80. 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.
81. Soman, P., P. H. Chung, A. P. Zhang, and S. Chen. Digital microfabrication of user-defined 3D microstructures in cell-laden hydrogels. Biotechnol. Bioeng. 110:3038–3047, 2013.
82. 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.
83. Williams, D. F. On the nature of biomaterials. Biomaterials. 30:5897–5909, 2009.
84. Williams, D. The continuing evolution of biomaterials. Biomaterials. 32:1–2, 2011.
85. Wust, S., M. E. Godla, R. Muller, and S. Hofmann. Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater. 10:630–640, 2014.
86. 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.
87. Xu, K., D. A. Cantu, Y. Fu, J. Kim, X. Zheng, P. Hematti, and W. J. Kao. Thiol-ene Michael-type formation of gelatin/poly(ethylene glycol) biomatrices for three-dimensional mesenchymal stromal/stem cell administration to cutaneous wounds. Acta Biomater. 9:8802–8814, 2013.
88. Zawaneh, P. N., S. P. Singh, R. F. Padera, P. W. Henderson, J. A. Spector, and D. Putnam. Design of an injectable synthetic and biodegradable surgical biomaterial. Proc. Natl. Acad. Sci. USA. 107:11014–11019, 2010.
89. Zhang, A. P., X. Qu, P. Soman, K. C. Hribar, J. W. Lee, S. Chen, and S. He. Rapid fabrication of complex 3D extracellular microenvironments by dynamic optical projection stereolithography. Adv. Mater. 24:4266–4270, 2012.
90. Zhang, C., X. Wen, N. R. Vyavahare, and T. Boland. Synthesis and characterization of biodegradable elastomeric polyurethane scaffolds fabricated by the inkjet technique. Biomaterials. 29:3781–3791, 2008.