Advanced Bioinks for 3D Printing: A Materials Science Perspective

Annals of Biomedical Engineering

Volumn 44, Issue 6, 2016, Pages 2090-2102

  Chimene, David ^a   Lennox, Kimberly K ^a   Kaunas, Roland R ^a   Gaharwar, Akhilesh K ^a,b,c  

^a Texas A M University   (United States)

^b Department of Electrical and Computer Engineering   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

3D printing; Bioinks; Hydrogels; Interpenetrating networks (IPNs); Nanomaterials; Supramolecular

Indexed keywords

CROSSLINKING; DESIGN; HYDROGELS; INTERPENETRATING POLYMER NETWORKS; NANOSTRUCTURED MATERIALS; PRINTING; SCAFFOLDS (BIOLOGY); SHEAR THINNING; SUPRAMOLECULAR CHEMISTRY;

3-D PRINTING; BIOINKS; CELLULAR FUNCTION; CYTOCOMPATIBILITY; ENCAPSULATED CELL; HIGH MECHANICAL STRENGTH; IMPROVED DESIGNS; SUPRAMOLECULAR;

3D PRINTERS;

BIOINKS; BIOMATERIAL; NANOCOMPOSITE; NANOMATERIAL; POLYMER; UNCLASSIFIED DRUG; INK;

BIOPRINTING; CELL ADHESION; CROSS LINKING; EXTRACELLULAR MATRIX; HUMAN; LEYDIG CELL; NANOBIOTECHNOLOGY; NANOENCAPSULATION; PRIORITY JOURNAL; PROCESS DESIGN; REVIEW; SUPRAMOLECULAR CHEMISTRY; SYNTHESIS; THREE DIMENSIONAL PRINTING; TISSUE ENGINEERING; ANIMAL; CHEMISTRY; DEVICES; PROCEDURES; TISSUE SCAFFOLD;

ANIMALS; BIOCOMPATIBLE MATERIALS; HUMANS; INK; PRINTING, THREE-DIMENSIONAL; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84968665431     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-016-1638-y     Document Type: Review

References (69)

1. Augst, A. D., H. J. Kong, and D. J. Mooney. Alginate hydrogels as biomaterials. Macromol. Biosci. 6:623–633, 2006.
2. Azagarsamy, M. A., and K. S. Anseth. Bioorthogonal click chemistry: an indispensable tool to create multifaceted cell culture scaffolds. ACS Macro Lett. 2:5–9, 2012.
3. Bakarich, S. E., R. Gorkin, M. I. H. Panhuis, and G. M. Spinks. 4D printing with mechanically robust, thermally actuating hydrogels. Macromol. Rapid Commun. 36:1211–1217, 2015.
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, and M. R. Dokmeci. Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 6:024105, 2014.
5. Bertassoni, L. E., M. Cecconi, V. Manoharan, M. Nikkhah, J. Hjortnaes, A. L. Cristino, G. Barabaschi, D. Demarchi, M. R. Dokmeci, and Y. Yang. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14:2202–2211, 2014.
6. Bhattacharjee, T., S. M. Zehnder, K. G. Rowe, S. Jain, R. M. Nixon, W. G. Sawyer, and T. E. Angelini. Writing in the granular gel medium. Sci. Adv. 1:e1500655, 2015.
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. Carrow, J. K., and A. K. Gaharwar. Bioinspired polymeric nanocomposites for regenerative medicine. Macromol. Chem. Phys. 216:248–264, 2015.
9. Chen, Q., H. Chen, L. Zhu, and J. Zheng. Fundamentals of double network hydrogels. J Mater Chem B 3:3654–3676, 2015.
10. Chen, Q., L. Zhu, L. Huang, H. Chen, K. Xu, Y. Tan, P. Wang, and J. Zheng. Fracture of the physically cross-linked first network in hybrid double network hydrogels. Macromolecules 47:2140–2148, 2014.
11. Chimene, D., D. L. Alge, and A. K. Gaharwar. Two-dimensional nanomaterials for biomedical applications: emerging trends and future prospects. Adv. Mater. 27:7261–7284, 2015.
12. Chung, J. H., S. Naficy, Z. Yue, R. Kapsa, A. Quigley, S. E. Moulton, and G. G. Wallace. Bio-ink properties and printability for extrusion printing living cells. Biomater. Sci. 1:763–773, 2013.
13. Discher, D. E., D. J. Mooney, and P. W. Zandstra. Growth factors, matrices, and forces combine and control stem cells. Science 324:1673–1677, 2009.
14. Duan, B., E. Kapetanovic, L. A. Hockaday, and J. T. Butcher. Three-dimensional printed trileaflet valve conduits using biological hydrogels and human valve interstitial cells. Acta Biomater. 10:1836–1846, 2014.
15. Durmus, N. G., S. Tasoglu, and U. Demirci. Bioprinting: functional droplet networks. Nat. Mater. 12:478–479, 2013.
16. Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matrix elasticity directs stem cell lineage specification. Cell 126:677–689, 2006.
17. Fisher, O. Z., A. Khademhosseini, R. Langer, and N. A. Peppas. Bioinspired materials for controlling stem cell fate. Acc. Chem. Res. 43:419–428, 2010.
18. Gaharwar, A. K., A. Arpanaei, T. L. Andresen, and A. Dolatshahi-Pirouz. 3D biomaterial microarrays for regenerative medicine: current state-of-the-art, emerging directions and future trends. Adv. Mater. 28:771–781, 2016.
19. Gaharwar, A. K., R. K. Avery, A. Assmann, A. Paul, G. H. McKinley, A. Khademhosseini, and B. D. Olsen. Shear-thinning nanocomposite hydrogels for the treatment of hemorrhage. ACS Nano 8:9833–9842, 2014.
20. Gaharwar, A. K., N. A. Peppas, and A. Khademhosseini. Nanocomposite hydrogels for biomedical applications. Biotechnol. Bioeng. 111:441–453, 2014.
21. Gaharwar, A. K., C. P. Rivera, C.-J. Wu, and G. Schmidt. Transparent, elastomeric and tough hydrogels from poly (ethylene glycol) and silicate nanoparticles. Acta Biomater. 7:4139–4148, 2011.
22. Gao, G., A. F. Schilling, T. Yonezawa, J. Wang, G. Dai, and X. Cui. Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol. J. 9:1304–1311, 2014.
23. Gasperini, L., J. F. Mano, and R. L. Reis. Natural polymers for the microencapsulation of cells. J. R. Soc. Interface 11:20140817, 2014.
24. Goenka, S., V. Sant, and S. Sant. Graphene-based nanomaterials for drug delivery and tissue engineering. J. Control. Release 173:75–88, 2014.
25. Guilak, F., D. M. Cohen, B. T. Estes, J. M. Gimble, W. Liedtke, and C. S. Chen. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5:17–26, 2009.
26. Haque, M. A., T. Kurokawa, and J. P. Gong. Super tough double network hydrogels and their application as biomaterials. Polymer 53:1805–1822, 2012.
27. Hart, L. R., J. L. Harries, B. W. Greenland, H. M. Colquhoun, and W. Hayes. Healable supramolecular polymers. Polymer Chemistry 4:4860–4870, 2013.
28. Highley, C. B., C. B. Rodell, and J. A. Burdick. Direct 3D printing of shear-thinning hydrogels into self-healing hydrogels. Adv. Mater. 27:5075–5079, 2015.
29. 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.
30. Hoffman, A. S. Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 64:18–23, 2012.
31. Hong, S., D. Sycks, H. F. Chan, S. Lin, G. P. Lopez, F. Guilak, K. W. Leong, and X. Zhao. 3D printing of highly stretchable and tough hydrogels into complex, cellularized structures. Adv. Mater. 27:4035–4040, 2015.
32. Huang, T., H. G. Xu, K. X. Jiao, L. P. Zhu, H. R. Brown, and H. L. Wang. A novel hydrogel with high mechanical strength: a macromolecular microsphere composite hydrogel. Adv. Mater. 19:1622–1626, 2007.
33. Jaiswal, M. K., J. R. Xavier, J. K. Carrow, P. Desai, D. Alge, and A. K. Gaharwar. Mechanically stiff nanocomposite hydrogels at ultralow nanoparticle content. ACS Nano 10:246–256, 2016.
34. 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.
35. Kang, H.-W., S. J. Lee, I. K. Ko, C. Kengla, J. J. Yoo, and A. Atala. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34:312–319, 2016.
36. Kerativitayanan, P., J. K. Carrow, and A. K. Gaharwar. Nanomaterials for engineering stem cell responses. Adv. Healthc Mater. 4:1600–1627, 2015.
37. Kesti, M., M. Müller, J. Becher, M. Schnabelrauch, M. D’Este, D. Eglin, and M. Zenobi-Wong. A versatile bioink for three-dimensional printing of cellular scaffolds based on thermally and photo-triggered tandem gelation. Acta Biomater. 11:162–172, 2015.
38. Kirchmajer, D. M., R. Gorkin, III, and M. I. H. Panhuis. An overview of the suitability of hydrogel-forming polymers for extrusion-based 3D-printing. J. Mater. Chem. B 3:4105–4117, 2015.
39. Kirchmajer, D. M., and M. I. H. Panhuis. Robust biopolymer based ionic-covalent entanglement hydrogels with reversible mechanical behaviour. J. Mater. Chem. B 2:4694–4702, 2014.
40. Kloxin, A. M., C. J. Kloxin, C. N. Bowman, and K. S. Anseth. Mechanical properties of cellularly responsive hydrogels and their experimental determination. Adv. Mater. 22:3484–3494, 2010.
41. 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.
42. Lee, V., G. Singh, J. P. Trasatti, C. Bjornsson, X. Xu, T. N. Tran, S.-S. Yoo, G. Dai, and P. Karande. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng. Part C Methods 20:473–484, 2013.
43. Malda, J., and J. Groll. A step towards clinical translation of biofabrication. Trends Biotechnol. 34:356, 2016.
44. Malda, J., J. Visser, F. P. Melchels, T. Jüngst, W. E. Hennink, W. J. Dhert, J. Groll, and D. W. Hutmacher. 25th anniversary article: engineering hydrogels for biofabrication. Adv. Mater. 25:5011–5028, 2013.
45. Markstedt, K., A. Mantas, I. Tournier, H. C. Martínez Ávila, D. Hägg, and P. Gatenholm. 3D Bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16:1489–1496, 2015.
46. Melchels, F. P., M. A. Domingos, T. J. Klein, J. Malda, P. J. Bartolo, and D. W. Hutmacher. Additive manufacturing of tissues and organs. Prog. Polym. Sci. 37:1079–1104, 2012.
47. Mironov, V., N. Reis, and B. Derby. Review: bioprinting: a beginning. Tissue Eng. 12:631–634, 2006.
48. 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.
49. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32:773–785, 2014.
50. Murphy, S. V., A. Skardal, and A. Atala. Evaluation of hydrogels for bio-printing applications. J. Biomed. Mater. Res. A 101A:272–284, 2013.
51. Parani, M., G. Lokhande, A. Singh, and A. K. Gaharwar. Engineered nanomaterials for infection control and healing acute and chronic wounds. ACS Appl. Mater. Interfaces 8:10049–10069, 2016.
52. Pati, F., J. Gantelius, and H. A. Svahn. 3D bioprinting of tissue/organ models. Angew. Chem. Int. Ed. 55:4650–4665, 2016.
53. 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.
54. Paul, A. Nanocomposite hydrogels: an emerging biomimetic platform for myocardial therapy and tissue engineering. Nanomedicine 10:1371–1374, 2015.
55. Peak, C. W., J. K. Carrow, A. Thakur, A. Singh, and A. K. Gaharwar. Elastomeric cell-laden nanocomposite microfibers for engineering complex tissues. Cell. Mol. Bioeng. 8:404–415, 2015.
56. Pereira, R. F., H. A. Almeida, and P. J. Bártolo. Drug delivery systems: advanced technologies potentially applicable in personalised treatmentBiofabrication Hydrogel Constr., Dordrecht: Springer, pp. 225–254, 2013.
57. Rowley, J. A., G. Madlambayan, and D. J. Mooney. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20:45–53, 1999.
58. 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.
59. Skardal, A., and A. Atala. Biomaterials for Integration with 3-D Bioprinting. Ann. Biomed. Eng. 43:730–746, 2015.
60. Slaughter, B. V., S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas. Hydrogels in regenerative medicine. Adv. Mater. 21:3307–3329, 2009.
61. Stanton, M., J. Samitier, and S. Sánchez. Bioprinting of 3D hydrogels. Lab Chip 15:3111–3115, 2015.
62. Suekama, T. C., J. Hu, T. Kurokawa, J. P. Gong, and S. H. Gehrke. Double-network strategy improves fracture properties of chondroitin sulfate networks. ACS Macro Lett. 2:137–140, 2013.
63. Thakur, T., J. R. Xavier, L. Cross, M. K. Jaiswal, E. Mondragon, R. Kaunas, and A. K. Gaharwar. Photocrosslinkable and elastomeric hydrogels for bone regeneration. J Biomed Mater Res A 104:879–888, 2016.
64. Thiele, J., Y. Ma, S. Bruekers, S. Ma, and W. T. Huck. 25th Anniversary article: designer hydrogels for cell cultures: a materials selection guide. Adv. Mater. 26:125–148, 2014.
65. Tibbitt, M. W., and K. S. Anseth. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol. Bioeng. 103:655–663, 2009.
66. Xavier, J. R., T. Thakur, P. Desai, M. K. Jaiswal, N. Sears, E. Cosgriff-Hernandez, R. Kaunas, and A. K. Gaharwar. Bioactive nanoengineered hydrogels for bone tissue engineering: a growth-factor-free approach. ACS Nano 9:3109–3118, 2015.
67. Xu, Y., and X. Wang. Application of 3D biomimetic models in drug delivery and regenerative medicine. Curr. Pharm. Des. 21:1618–1626, 2015.
68. Yang, L., X. Tan, Z. Wang, and X. Zhang. Supramolecular polymers: historical development, preparation, characterization, and functions. Chem. Rev. 115:7196–7239, 2015.
69. Zhu, W., X. Ma, M. Gou, D. Mei, K. Zhang, and S. Chen. 3D printing of functional biomaterials for tissue engineering. Curr. Opin. Biotechnol. 40:103–112, 2016.