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Materials as Bioinks and Bioink Design

  • Paula Camacho
  • Hafiz Busari
  • Kelly B. Seims
  • John W. Tolbert
  • Lesley W. ChowEmail author
Chapter

Abstract

This chapter summarizes the major concepts and recent progress in the design and formulation of bioinks for 3D bioprinting. Bioinks encompass cells and materials designed for processing by an automated biofabrication technique, such as direct-write, inkjet, stereolithography (SLA), or laser-induced forward transfer (LIFT) technologies, with each having its own requirements for material properties to fabricate specific tissue constructs. There are two major types of bioinks: (1) scaffold-free, consisting of cellular aggregates, and (2) scaffold-based, comprised of biomaterials with encapsulated cells. These bioinks can be composed of single materials or blends of multiple components to develop constructs tailored to preferred printing techniques and applications. Key parameters important in material selection include printability, mechanical properties, degradation, biochemical functionality, cell viability, and biocompatibility. Single-component hydrogels have limitations since properties that enhance cell viability and function often contrast with those that facilitate printing of mechanically robust constructs. More complex formulations, such as multi-material bioinks, interpenetrating networks, and nanocomposite bioinks, expand the range of properties and techniques that can be achieved for desired applications. Future directions will demonstrate how bioinks can be optimized and exploited to engineer native-like tissue constructs with spatially and temporally organized biochemical and biophysical cues and tissue-specific cell types.

Keywords

Bioink design Polymeric materials Hydrogels Cellular aggregates 

Notes

Acknowledgments

This work was supported by startup funds provided by Lehigh University. KBS also acknowledges the support through a President’s Scholarship from Lehigh University.

References

  1. 1.
    Groll J, Burdick JA, Cho D, Derby B, Gelinsky M, Heilshorn SC, Jüngst T, Malda J, Mironov VA, Nakayama K, Ovsianikov A, Sun W, Takeuchi S, Yoo JJ, Woodfield TBF (2018) A definition of bioinks and their distinction from biomaterial inks. Biofabrication 11:013001.  https://doi.org/10.1088/1758-5090/aaec52CrossRefPubMedGoogle Scholar
  2. 2.
    Achilli T-M, Meyer J, Morgan JR (2012) Advances in the formation, use and understanding of multi-cellular spheroids. Expert Opin Biol Ther 12:1347–1360.  https://doi.org/10.1517/14712598.2012.707181CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR (2009) Organ printing: tissue spheroids as building blocks. Biomaterials 30:2164–2174.  https://doi.org/10.1016/j.biomaterials.2008.12.084CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Cui X, Hartanto Y, Zhang H (2017) Advances in multicellular spheroids formation. J R Soc Interface 14:20160877.  https://doi.org/10.1098/rsif.2016.0877CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Rezende RA, Pereira FDAS, Kasyanov V, Kemmoku DT, Maia I, Da Silva JVL, Mironov V (2013) Scalable biofabrication of tissue spheroids for organ printing. Proc CIRP 5:276–281. doi:  https://doi.org/10.1016/j.procir.2013.01.054CrossRefGoogle Scholar
  6. 6.
    Liu W, Heinrich MA, Zhou Y, Akpek A, Hu N, Liu X, Guan X, Zhong Z, Jin X, Khademhosseini A, Zhang YS (2017) Extrusion bioprinting of shear-thinning gelatin methacryloyl bioinks. Adv Healthc Mater 6:1–11.  https://doi.org/10.1002/adhm.201601451CrossRefGoogle Scholar
  7. 7.
    Yipeng J, Yongde X, Yuanyi W, Jilei S, Jiaxiang G, Jiangping G, Yong Y (2017) Microtissues enhance smooth muscle differentiation and cell viability of hADSCs for three dimensional bioprinting. Front Physiol 8:1–10.  https://doi.org/10.3389/fphys.2017.00534CrossRefGoogle Scholar
  8. 8.
    Ozbolat IT (2015) Scaffold-based or scaffold-free bioprinting: competing or complementing approaches? J Nanotechnol Eng Med 6:024701.  https://doi.org/10.1115/1.4030414CrossRefGoogle Scholar
  9. 9.
    Moldovan NI (2018) Progress in scaffold-free bioprinting for cardiovascular medicine. J Cell Mol Med 22:2964–2969.  https://doi.org/10.1111/jcmm.13598CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Axpe E, Oyen M (2016) Applications of alginate-based bioinks in 3D bioprinting. Int J Mol Sci 17:1976.  https://doi.org/10.3390/ijms17121976CrossRefPubMedCentralGoogle Scholar
  11. 11.
    Yang X, Lu Z, Wu H, Li W, Zheng L, Zhao J (2018) Collagen-alginate as bioink for three-dimensional (3D) cell printing based cartilage tissue engineering. Mater Sci Eng C 83:195–201.  https://doi.org/10.1016/j.msec.2017.09.002CrossRefGoogle Scholar
  12. 12.
    England S, Rajaram A, Schreyer DJ, Chen X (2017) Bioprinted fibrin-factor XIII-hyaluronate hydrogel scaffolds with encapsulated Schwann cells and their in vitro characterization for use in nerve regeneration. Bioprinting 5:1–9.  https://doi.org/10.1016/j.bprint.2016.12.001CrossRefGoogle Scholar
  13. 13.
    Zhang K, Fu Q, Yoo J, Chen X, Chandra P, Mo X, Song L, Atala A, Zhao W (2017) 3D bioprinting of urethra with PCL/PLCL blend and dual autologous cells in fibrin hydrogel: an in vitro evaluation of biomimetic mechanical property and cell growth environment. Acta Biomater 50:154–164.  https://doi.org/10.1016/j.actbio.2016.12.008CrossRefPubMedGoogle Scholar
  14. 14.
    Sultan S, Siqueira G, Zimmermann T, Mathew AP (2017) 3D printing of nano-cellulosic biomaterials for medical applications. Curr Opin Biomed Eng 2:29–34.  https://doi.org/10.1016/j.cobme.2017.06.002CrossRefGoogle Scholar
  15. 15.
    Das S, Pati F, Choi YJ, Rijal G, Shim JH, Kim SW, Ray AR, Cho DW, Ghosh S (2015) Bioprintable, cell-laden silk fibroin-gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater 11:233–246.  https://doi.org/10.1016/j.actbio.2014.09.023CrossRefPubMedGoogle Scholar
  16. 16.
    Jose RR, Rodriguez MJ, Dixon TA, Omenetto F, Kaplan DL (2016) Evolution of bioinks and additive manufacturing technologies for 3D bioprinting. ACS Biomater Sci Eng 2:1662–1678.  https://doi.org/10.1021/acsbiomaterials.6b00088CrossRefGoogle Scholar
  17. 17.
    Shin M, Galarraga JH, Kwon MY, Lee H, Burdick JA (2018) Gallol-derived ECM-mimetic adhesive bioinks exhibiting temporal shear-thinning and stabilization behavior. Acta Biomater. pii: S1742-7061(18)30627-5.  https://doi.org/10.1016/J.ACTBIO.2018.10.028
  18. 18.
    Pati F, Jang J, Ha DH, Won Kim S, Rhie JW, Shim JH, Kim DH, Cho DW (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:1–11.  https://doi.org/10.1038/ncomms4935CrossRefGoogle Scholar
  19. 19.
    Donderwinkel I, van Hest JCM, Cameron NR (2017) Bio-inks for 3D bioprinting: recent advances and future prospects. Polym Chem 8:4451–4471. doi:  https://doi.org/10.1039/C7PY00826KCrossRefGoogle Scholar
  20. 20.
    Saunders RE, Derby B (2014) Inkjet printing biomaterials for tissue engineering: bioprinting. Int Mater Rev 59:430–448.  https://doi.org/10.1179/1743280414Y.0000000040CrossRefGoogle Scholar
  21. 21.
    Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT (2017) The bioink: a comprehensive review on bioprintable materials. Biotechnol Adv 35:217–239.  https://doi.org/10.1016/j.biotechadv.2016.12.006CrossRefPubMedGoogle Scholar
  22. 22.
    Skoog SA, Goering PL, Narayan RJ (2014) Stereolithography in tissue engineering. J Mater Sci Mater Med 25:845–856.  https://doi.org/10.1007/s10856-013-5107-yCrossRefPubMedGoogle Scholar
  23. 23.
    Ji S, Guvendiren M (2017) Recent advances in bioink design for 3D bioprinting of tissues and organs. Front Bioeng Biotechnol 5:1–8.  https://doi.org/10.3389/fbioe.2017.00023CrossRefGoogle Scholar
  24. 24.
    Duan B, Kapetanovic E, Hockaday LA, Butcher JT (2014) Three-dimensional printed trileaflet valve conduits using biological hydrogels and human valve interstitial cells. Acta Biomater 10:1836–1846.  https://doi.org/10.1016/j.actbio.2013.12.005CrossRefPubMedGoogle Scholar
  25. 25.
    Vafaei S, Tuck C, Ashcroft I, Wildman R (2016) Surface microstructuring to modify wettability for 3D printing of nano-filled inks. Chem Eng Res Des 109:414–420.  https://doi.org/10.1016/j.cherd.2016.02.004CrossRefGoogle Scholar
  26. 26.
    Mandrycky C, Wang Z, Kim K, Kim DH (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34:422–434.  https://doi.org/10.1016/j.biotechadv.2015.12.011CrossRefPubMedGoogle Scholar
  27. 27.
    Xu C, Zhang M, Huang Y, Ogale A, Fu J, Markwald RR (2014) Study of droplet formation process during drop-on-demand inkjetting of living cell-laden bioink. Langmuir 30:9130–9138.  https://doi.org/10.1021/la501430xCrossRefPubMedGoogle Scholar
  28. 28.
    Rutz AL, Hyland KE, Jakus AE, Burghardt WR, Shah RN (2015) A multimaterial bioink method for 3D printing tunable, cell-compatible hydrogels. Adv Mater 27:1607–1614.  https://doi.org/10.1002/adma.201405076CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Jakus AE, Rutz AL, Shah RN (2016) Advancing the field of 3D biomaterial printing. Biomed Mater 11:014102.  https://doi.org/10.1088/1748-6041/11/1/014102CrossRefPubMedGoogle Scholar
  30. 30.
    Wüst S, Godla ME, Müller R, Hofmann S (2014) Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater 10:630–640.  https://doi.org/10.1016/j.actbio.2013.10.016CrossRefPubMedGoogle Scholar
  31. 31.
    Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689.  https://doi.org/10.1016/j.cell.2006.06.044CrossRefPubMedGoogle Scholar
  32. 32.
    Ghasemi-Mobarakeh L (2015) Structural properties of scaffolds: crucial parameters towards stem cells differentiation. World J Stem Cells 7:728.  https://doi.org/10.4252/wjsc.v7.i4.728CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Velasco MA, Narváez-Tovar CA, Garzón-Alvarado DA (2015) Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. Biomed Res Int 2015:1–21.  https://doi.org/10.1155/2015/729076CrossRefGoogle Scholar
  34. 34.
    Freeman FE, Kelly DJ (2017) Tuning alginate bioink stiffness and composition for controlled growth factor delivery and to spatially direct MSC Fate within bioprinted tissues. Sci Rep 7:1–12.  https://doi.org/10.1038/s41598-017-17286-1CrossRefGoogle Scholar
  35. 35.
    Jungst T, Smolan W, Schacht K, Scheibel T, Groll J (2016) Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev 116:1496–1539.  https://doi.org/10.1021/acs.chemrev.5b00303CrossRefPubMedGoogle Scholar
  36. 36.
    Parsa S, Gupta M, Loizeau F, Cheung KC (2010) Effects of surfactant and gentle agitation on inkjet dispensing of living cells. Biofabrication 2:025003.  https://doi.org/10.1088/1758-5082/2/2/025003CrossRefPubMedGoogle Scholar
  37. 37.
    Gopinathan J, Noh I (2018) Recent trends in bioinks for 3D printing. Biomater Res 22:11.  https://doi.org/10.1186/s40824-018-0122-1CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Chimene D, Lennox KK, Kaunas RR, Gaharwar AK (2016) Advanced bioinks for 3D printing: a materials science perspective. Ann Biomed Eng 44:2090–2102.  https://doi.org/10.1007/s10439-016-1638-yCrossRefPubMedGoogle Scholar
  39. 39.
    Mano JF, Silva GA, Azevedo HS, Malafaya PB, Sousa RA, Silva SS, Boesel LF, Oliveira JM, Santos TC, Marques AP, Neves NM, Reis RL (2007) Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface 4:999–1030.  https://doi.org/10.1098/rsif.2007.0220CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Gordon TD, Schloesser L, Humphries DE, Spector M (2004) Effects of the degradation rate of collagen matrices on articular chondrocyte proliferation and biosynthesis in vitro. Tissue Eng 10(7–8):1287–1295CrossRefGoogle Scholar
  41. 41.
    Diniz IMA, Chen C, Xu X, Ansari S, Zadeh HH, Marques MM, Shi S, Moshaverinia A (2015) Pluronic F-127 hydrogel as a promising scaffold for encapsulation of dental-derived mesenchymal stem cells. J Mater Sci Mater Med 26:1–10.  https://doi.org/10.1007/s10856-015-5493-4CrossRefGoogle Scholar
  42. 42.
    Guarino V, Caputo T, Altobelli R, Ambrosio L (2015) Degradation properties and metabolic activity of alginate and chitosan polyelectrolytes for drug delivery and tissue engineering applications. AIMS Mater Sci 2:497–502.  https://doi.org/10.3934/matersci.2015.4.497CrossRefGoogle Scholar
  43. 43.
    Kong HJ, Kaigler D, Kim K, Mooney DJ (2004) Controlling rigidity and degradation of alginate hydrogels via molecular weight distribution. Biomacromolecules 5:1720–1727.  https://doi.org/10.1021/bm049879rCrossRefPubMedGoogle Scholar
  44. 44.
    Parak A, Pradeep P, du Toit LC, Kumar P, Choonara YE, Pillay V (2018) Functionalizing bioinks for 3D bioprinting applications. Drug Discov Today 00:1–8. doi:  https://doi.org/10.1016/j.drudis.2018.09.012CrossRefGoogle Scholar
  45. 45.
    Hersel U, Dahmen C, Kessler H (2003) RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24:4385–4415.  https://doi.org/10.1016/S0142-9612(03)00343-0CrossRefPubMedGoogle Scholar
  46. 46.
    Kundu J, Poole-Warren LA, Martens P, Kundu SC (2012) Silk fibroin/poly(vinyl alcohol) photocrosslinked hydrogels for delivery of macromolecular drugs. Acta Biomater 8:1720–1729.  https://doi.org/10.1016/j.actbio.2012.01.004CrossRefPubMedGoogle Scholar
  47. 47.
    De Maria C, Vozzi G, Moroni L (2017) Multimaterial, heterogeneous, and multicellular three-dimensional bioprinting. MRS Bull 42:578–584. doi:  https://doi.org/10.1557/mrs.2017.165CrossRefGoogle Scholar
  48. 48.
    Aguado BA, Mulyasasmita W, Su J, Lampe KJ, Heilshorn SC (2012) Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers. Tissue Eng Part A 18:806–815.  https://doi.org/10.1089/ten.tea.2011.0391CrossRefPubMedGoogle Scholar
  49. 49.
    Rodriguez MJ, Brown J, Giordano J, Lin SJ, Omenetto FG, Kaplan DL (2017) Dimensional (3D) printing with in vitro and in vivo assessments. Biomaterials 117:105–115.  https://doi.org/10.1016/j.biomaterials.2016.11.046.SilkCrossRefPubMedGoogle Scholar
  50. 50.
    Cui H, Nowicki M, Fisher JP, Zhang LG (2017) 3D bioprinting for organ regeneration. Adv Healthc Mater 6:1601118.  https://doi.org/10.1002/adhm.201601118CrossRefGoogle Scholar
  51. 51.
    Norotte C, Marga FS, Niklason LE, Forgacs G (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917.  https://doi.org/10.1016/j.biomaterials.2009.06.034CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Seliktar D (2012) Designing cell-compatible hydrogels for biomedical applications. Science 336:1124–1128.  https://doi.org/10.1126/science.1214804CrossRefPubMedGoogle Scholar
  53. 53.
    Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351.  https://doi.org/10.1016/S0142-9612(03)00340-5CrossRefPubMedGoogle Scholar
  54. 54.
    Zhu J, Marchant RE (2011) Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices 8:607–626.  https://doi.org/10.1586/erd.11.27CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Dubbin K, Hori Y, Lewis KK, Heilshorn SC (2016) Dual-stage crosslinking of a gel-phase bioink improves cell viability and homogeneity for 3D bioprinting. Adv Healthc Mater 5:2488–2492.  https://doi.org/10.1002/adhm.201600636CrossRefPubMedGoogle Scholar
  56. 56.
    Ouyang L, Highley CB, Rodell CB, Sun W, Burdick JA (2016) 3D Printing of shear-thinning hyaluronic acid hydrogels with secondary cross-linking. ACS Biomater Sci Eng 2:1743–1751.  https://doi.org/10.1021/acsbiomaterials.6b00158CrossRefGoogle Scholar
  57. 57.
    Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A (2010) Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31:5536–5544.  https://doi.org/10.1016/j.biomaterials.2010.03.064CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Zheng Z, Wu J, Liu M, Wang H, Li C, Rodriguez MJ, Li G, Wang X, Kaplan DL (2018) 3D bioprinting of self-standing silk-based bioink. Adv Healthc Mater 7:1701026.  https://doi.org/10.1002/adhm.201701026CrossRefGoogle Scholar
  59. 59.
    Gioffredi E, Boffito M, Calzone S, Giannitelli SM, Rainer A, Trombetta M, Mozetic P, Chiono V (2016) Pluronic F127 hydrogel characterization and biofabrication in cellularized constructs for tissue engineering applications. Proc CIRP 49:125–132.  https://doi.org/10.1016/j.procir.2015.11.001CrossRefGoogle Scholar
  60. 60.
    Guvendiren M, Molde J, Soares RMD, Kohn J (2016) Designing biomaterials for 3D printing. ACS Biomater Sci Eng 2:1679–1693.  https://doi.org/10.1021/acsbiomaterials.6b00121CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Zhang X-Z, Wu D-Q, Chu C-C (2004) Synthesis, characterization and controlled drug release of thermosensitive IPN–PNIPAAm hydrogels. Biomaterials 25:3793–3805.  https://doi.org/10.1016/j.biomaterials.2003.10.065CrossRefPubMedGoogle Scholar
  62. 62.
    Thomas D, Jessop Z, Whitaker I (2018) 3D bioprinting for reconstructive surgery: techniques and applicationsGoogle Scholar
  63. 63.
    Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJA, Groll J, Hutmacher DW (2013) 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater 25:5011–5028.  https://doi.org/10.1002/adma.201302042CrossRefPubMedGoogle Scholar
  64. 64.
    Kreimendahl F, Köpf M, Thiebes AL, Duarte Campos DF, Blaeser A, Schmitz-Rode T, Apel C, Jockenhoevel S, Fischer H (2017) Three-dimensional printing and angiogenesis: tailored agarose-type I collagen blends comprise three-dimensional printability and angiogenesis potential for tissue-engineered substitutes. Tissue Eng Part C Methods 23:604–615.  https://doi.org/10.1089/ten.tec.2017.0234CrossRefPubMedGoogle Scholar
  65. 65.
    Forget A, Blaeser A, Miessmer F, Köpf M, Campos DFD, Voelcker NH, Blencowe A, Fischer H, Shastri VP (2017) Mechanically tunable bioink for 3D bioprinting of human cells. Adv Healthc Mater 6:1700255.  https://doi.org/10.1002/adhm.201700255CrossRefGoogle Scholar
  66. 66.
    Augst AD, Kong HJ, Mooney DJ (2006) Alginate hydrogels as biomaterials. Macromol Biosci 6:623–633.  https://doi.org/10.1002/mabi.200600069CrossRefPubMedGoogle Scholar
  67. 67.
    Chung JHY, Naficy S, Yue Z, Kapsa R, Quigley A, Moulton SE, Wallace GG (2013) Bio-ink properties and printability for extrusion printing living cells. Biomater Sci 1:763.  https://doi.org/10.1039/c3bm00012eCrossRefGoogle Scholar
  68. 68.
    Becker TA, Kipke DR (2002) Flow properties of liquid calcium alginate polymer injected through medical microcatheters for endovascular embolization. J Biomed Mater Res 61:533–540.  https://doi.org/10.1002/jbm.10202CrossRefPubMedGoogle Scholar
  69. 69.
    Kong H (2003) Designing alginate hydrogels to maintain viability of immobilized cells. Biomaterials 24:4023–4029.  https://doi.org/10.1016/S0142-9612(03)00295-3CrossRefPubMedGoogle Scholar
  70. 70.
    Kong H-J, Lee KY, Mooney DJ (2002) Decoupling the dependence of rheological/mechanical properties of hydrogels from solids concentration. Polymer (Guildf) 43:6239–6246.  https://doi.org/10.1016/S0032-3861(02)00559-1CrossRefGoogle Scholar
  71. 71.
    Kuo CK, Ma PX (2001) Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: Part 1. Structure, gelation rate and mechanical properties. Biomaterials 22:511–521.  https://doi.org/10.1016/S0142-9612(00)00201-5CrossRefPubMedGoogle Scholar
  72. 72.
    Jia J, Richards DJ, Pollard S, Tan Y, Rodriguez J, Visconti RP, Trusk TC, Yost MJ, Yao H, Markwald RR, Mei Y (2014) Engineering alginate as bioink for bioprinting. Acta Biomater 10:4323–4331.  https://doi.org/10.1016/j.actbio.2014.06.034CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Ferreira AM, Gentile P, Chiono V, Ciardelli G (2012) Collagen for bone tissue regeneration. Acta Biomater 8:3191–3200.  https://doi.org/10.1016/j.actbio.2012.06.014CrossRefPubMedGoogle Scholar
  74. 74.
    Billiet T, Gevaert E, De Schryver T, Cornelissen M, Dubruel P (2014) The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials 35:49–62. doi:  https://doi.org/10.1016/j.biomaterials.2013.09.078CrossRefPubMedGoogle Scholar
  75. 75.
    Gruene M, Pflaum M, Hess C, Diamantouros S, Schlie S, Deiwick A, Koch L, Wilhelmi M, Jockenhoevel S, Haverich A, Chichkov B (2011) Laser printing of three-dimensional multicellular arrays for studies of cell–cell and cell–environment interactions. Tissue Eng Part C Methods 17:973–982.  https://doi.org/10.1089/ten.tec.2011.0185CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Highley CB, Prestwich GD, Burdick JA (2016) Recent advances in hyaluronic acid hydrogels for biomedical applications. Curr Opin Biotechnol 40:35–40.  https://doi.org/10.1016/j.copbio.2016.02.008CrossRefPubMedGoogle Scholar
  77. 77.
    Poldervaart MT, Goversen B, de Ruijter M, Abbadessa A, Melchels FPW, Öner FC, Dhert WJA, Vermonden T, Alblas J (2017) 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS One 12:1–15. doi:  https://doi.org/10.1371/journal.pone.0177628CrossRefGoogle Scholar
  78. 78.
    Skardal A, Zhang J, Prestwich GD (2010) Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 31:6173–6181.  https://doi.org/10.1016/j.biomaterials.2010.04.045CrossRefPubMedGoogle Scholar
  79. 79.
    Nguyen D, Hägg DA, Forsman A, Ekholm J, Nimkingratana P, Brantsing C, Kalogeropoulos T, Zaunz S, Concaro S, Brittberg M, Lindahl A, Gatenholm P, Enejder A, Simonsson S (2017) Cartilage tissue engineering by the 3D bioprinting of ips cells in a nanocellulose/alginate bioink. Sci Rep 7:658.  https://doi.org/10.1038/s41598-017-00690-yCrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Markstedt K, Mantas A, Tournier I, Martínez Ávila H, Hägg D, Gatenholm P (2015) 3D bioprinting human chondrocytes with nanocellulose–alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16:1489–1496.  https://doi.org/10.1021/acs.biomac.5b00188CrossRefPubMedGoogle Scholar
  81. 81.
    Lott JR, McAllister JW, Arvidson SA, Bates FS, Lodge TP (2013) Fibrillar structure of methylcellulose hydrogels. Biomacromolecules 14:2484–2488.  https://doi.org/10.1021/bm400694rCrossRefPubMedGoogle Scholar
  82. 82.
    Kobayashi K, Huang C, Lodge TP (1999) Thermoreversible gelation of aqueous methylcellulose solutions. Macromolecules 32:7070–7077.  https://doi.org/10.1021/ma990242nCrossRefGoogle Scholar
  83. 83.
    Thirumala S, Gimble J, Devireddy R (2013) Methylcellulose based thermally reversible hydrogel system for tissue engineering applications. Cell 2:460–475.  https://doi.org/10.3390/cells2030460CrossRefGoogle Scholar
  84. 84.
    Kundu B, Rajkhowa R, Kundu SC, Wang X (2013) Silk fibroin biomaterials for tissue regenerations. Adv Drug Deliv Rev 65:457–470.  https://doi.org/10.1016/j.addr.2012.09.043CrossRefPubMedGoogle Scholar
  85. 85.
    Floren M, Bonani W, Dharmarajan A, Motta A, Migliaresi C, Tan W (2016) Human mesenchymal stem cells cultured on silk hydrogels with variable stiffness and growth factor differentiate into mature smooth muscle cell phenotype. Acta Biomater 31:156–166.  https://doi.org/10.1016/j.actbio.2015.11.051CrossRefPubMedGoogle Scholar
  86. 86.
    Rodriguez MJ, Brown J, Giordano J, Lin SJ, Omenetto FG, Kaplan DL (2017) Silk based bioinks for soft tissue reconstruction using 3-dimensional (3D) printing with in vitro and in vivo assessments. Biomaterials 117:105–115.  https://doi.org/10.1016/j.biomaterials.2016.11.046CrossRefPubMedGoogle Scholar
  87. 87.
    Wang X, Partlow B, Liu J, Zheng Z, Su B, Wang Y, Kaplan DL (2015) Injectable silk-polyethylene glycol hydrogels. Acta Biomater 12:51–61.  https://doi.org/10.1016/j.actbio.2014.10.027CrossRefPubMedGoogle Scholar
  88. 88.
    Frantz C, Stewart KM, Weaver VM (2010) The extracellular matrix at a glance. J Cell Sci 123:4195–4200.  https://doi.org/10.1242/jcs.023820CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Jung JP, Bhuiyan DB, Ogle BM (2016) Solid organ fabrication: comparison of decellularization to 3D bioprinting. Biomater Res 20:27.  https://doi.org/10.1186/s40824-016-0074-2CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Jang J, Park HJ, Kim SW, Kim H, Park JY, Na SJ, Kim HJ, Park MN, Choi SH, Park SH, Kim SW, Kwon SM, Kim PJ, Cho DW (2017) 3D printed complex tissue construct using stem cell-laden decellularized extracellular matrix bioinks for cardiac repair. Biomaterials 112:264–274.  https://doi.org/10.1016/j.biomaterials.2016.10.026CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Lutolf MP, Hubbell JA (2005) Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23:47–55.  https://doi.org/10.1038/nbt1055CrossRefPubMedGoogle Scholar
  92. 92.
    Kang HW, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A (2016) A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 34:312–319.  https://doi.org/10.1038/nbt.3413CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Khattak SF, Bhatia SR, Roberts SC (2005) Pluronic F127 as a cell encapsulation material: utilization of membrane-stabilizing agents. Tissue Eng 11:974–983.  https://doi.org/10.1089/ten.2005.11.974CrossRefPubMedGoogle Scholar
  94. 94.
    Müller M, Becher J, Schnabelrauch M, Zenobi-Wong M (2015) Nanostructured pluronic hydrogels as bioinks for 3D bioprinting. Biofabrication 7(3):035006.  https://doi.org/10.1088/1758-5090/7/3/035006CrossRefPubMedGoogle Scholar
  95. 95.
    Hockaday LA, Kang KH, Colangelo NW, Cheung PYC, Duan B, Malone E, Wu J, Girardi LN, Bonassar LJ, Lipson H, Chu CC, Butcher JT (2012) Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 4:035005.  https://doi.org/10.1088/1758-5082/4/3/035005CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Gao G, Yonezawa T, Hubbell K, Dai G, Cui X (2015) Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol J 10:1568–1577.  https://doi.org/10.1002/biot.201400635CrossRefPubMedGoogle Scholar
  97. 97.
    Kesti M, Müller M, Becher J, Schnabelrauch M, D’Este M, Eglin D, Zenobi-Wong M (2015) A versatile bioink for three-dimensional printing of cellular scaffolds based on thermally and photo-triggered tandem gelation. Acta Biomater 11:162–172.  https://doi.org/10.1016/j.actbio.2014.09.033CrossRefPubMedGoogle Scholar
  98. 98.
    Wu D, Yu Y, Tan J, Huang L, Luo B, Lu L, Zhou C (2018) 3D bioprinting of gellan gum and poly (ethylene glycol) diacrylate based hydrogels to produce human-scale constructs with high-fidelity. Mater Des 160:486–495.  https://doi.org/10.1016/j.matdes.2018.09.040CrossRefGoogle Scholar
  99. 99.
    Wilson SA, Cross LM, Peak CW, Gaharwar AK (2017) Shear-thinning and thermo-reversible nanoengineered inks for 3D bioprinting. ACS Appl Mater Interfaces 9:43449–43458.  https://doi.org/10.1021/acsami.7b13602CrossRefPubMedGoogle Scholar
  100. 100.
    Bertassoni LE, Cardoso JC, Manoharan V, Cristino AL, Bhise NS, Araujo WA, Zorlutuna P, Vrana NE, Ghaemmaghami AM, Dokmeci MR, Khademhosseini A (2014) Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 6:024105.  https://doi.org/10.1088/1758-5082/6/2/024105CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Shim JH, Kim JY, Park M, Park J, Cho DW (2011) Development of a hybrid scaffold with synthetic biomaterials and hydrogel using solid freeform fabrication technology. Biofabrication 3:034102.  https://doi.org/10.1088/1758-5082/3/3/034102CrossRefPubMedGoogle Scholar
  102. 102.
    Hinton TJ, Jallerat Q, Palchesko RN, Park JH, Grodzicki MS, Shue H-J, Ramadan MH, Hudson AR, Feinberg AW (2015) Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv 1:e1500758.  https://doi.org/10.1126/sciadv.1500758CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Bhattacharjee T, Zehnder SM, Rowe KG, Jain S, Nixon RM, Sawyer WG, Angelini TE (2015) Writing in the granular gel medium. Sci Adv 1:e1500655.  https://doi.org/10.1126/sciadv.1500655CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Jenkins AD, Kratochvíl P, Stepto RFT, Suter UW (1996) Glossary of basic terms in polymer science (IUPAC Recommendations 1996). Pure Appl Chem 68:2287–2311.  https://doi.org/10.1351/pac199668122287CrossRefGoogle Scholar
  105. 105.
    Lin P, Ma S, Wang X, Zhou F (2015) Molecularly engineered dual-crosslinked hydrogel with ultrahigh mechanical strength, toughness, and good self-recovery. Adv Mater 27:2054–2059.  https://doi.org/10.1002/adma.201405022CrossRefPubMedGoogle Scholar
  106. 106.
    Chen H, Liu Y, Ren B, Zhang Y, Ma J, Xu L, Chen Q, Zheng J (2017) Super bulk and interfacial toughness of physically crosslinked double-network hydrogels. Adv Funct Mater 27:1–10.  https://doi.org/10.1002/adfm.201703086CrossRefGoogle Scholar
  107. 107.
    Pulieri E, Chiono V, Ciardelli G, Vozzi G, Ahluwalia A, Domenici C, Vozzi F, Giusti P (2008) Chitosan/gelatin blends for biomedical applications. J Biomed Mater Res A 86A:311–322.  https://doi.org/10.1002/jbm.a.31492CrossRefGoogle Scholar
  108. 108.
    Naseri N, Deepa B, Mathew AP, Oksman K, Girandon L (2016) Nanocellulose-based interpenetrating polymer network (IPN) hydrogels for cartilage applications. Biomacromolecules 17:3714–3723.  https://doi.org/10.1021/acs.biomac.6b01243CrossRefPubMedGoogle Scholar
  109. 109.
    Hoare TR, Kohane DS (2008) Hydrogels in drug delivery: progress and challenges. Polymer (Guildf) 49:1993–2007.  https://doi.org/10.1016/j.polymer.2008.01.027CrossRefGoogle Scholar
  110. 110.
    Reis AV, Guilherme MR, Moia TA, Mattoso LHC, Muniz EC, Tambourgi EB (2008) Synthesis and characterization of a starch-modified hydrogel as potential carrier for drug delivery system. J Polym Sci A Polym Chem 46:2567–2574.  https://doi.org/10.1002/pola.22588CrossRefGoogle Scholar
  111. 111.
    Muzzarelli RAA (2009) Genipin-crosslinked chitosan hydrogels as biomedical and pharmaceutical aids. Carbohydr Polym 77:1–9.  https://doi.org/10.1016/j.carbpol.2009.01.016CrossRefGoogle Scholar
  112. 112.
    Bajaj P, Schweller RM, Khademhosseini A, West JL, Bashir R (2014) 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu Rev Biomed Eng 16:247–276.  https://doi.org/10.1146/annurev-bioeng-071813-105155CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Roland CM (2015) Interpenetrating polymer networks (IPN): structure and mechanical behavior. In: Encyclopedia of polymeric nanomaterials. Springer, Berlin, pp 1004–1011CrossRefGoogle Scholar
  114. 114.
    Pescosolido L, Schuurman W, Malda J, Matricardi P, Alhaique F, Coviello T, van Weeren PR, Dhert WJA, Hennink WE, Vermonden T (2011) Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting. Biomacromolecules 12:1831–1838. doi:  https://doi.org/10.1021/bm200178wCrossRefPubMedGoogle Scholar
  115. 115.
    Chatterjee U, Jewrajka SK, Guha S (2009) Dispersion of functionalized silver nanoparticles in polymer matrices: stability, characterization, and physical properties. Polym Compos 30:827–834.  https://doi.org/10.1002/pc.20655CrossRefGoogle Scholar
  116. 116.
    Liu HL, Dai SA, Fu KY, Hsu SH (2010) Antibacterial properties of silver nanoparticles in three different sizes and their nanocomposites with a new waterborne polyurethane. Int J Nanomed 5:1017–1028.  https://doi.org/10.2147/IJN.S14572CrossRefGoogle Scholar
  117. 117.
    Deka H, Karak N, Kalita RD, Buragohain AK (2010) Bio-based thermostable, biodegradable and biocompatible hyperbranched polyurethane/Ag nanocomposites with antimicrobial activity. Polym Degrad Stab 95:1509–1517.  https://doi.org/10.1016/j.polymdegradstab.2010.06.017CrossRefGoogle Scholar
  118. 118.
    Zhu K, Shin SR, van Kempen T, Li Y-C, Ponraj V, Nasajpour A, Mandla S, Hu N, Liu X, Leijten J, Lin Y-D, Hussain MA, Zhang YS, Tamayol A, Khademhosseini A (2017) Gold nanocomposite bioink for printing 3D cardiac constructs. Adv Funct Mater 27:1605352. doi:  https://doi.org/10.1002/adfm.201605352CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Cobley CM, Chen J, Cho EC, Wang LV, Xia Y (2011) Gold nanostructures: a class of multifunctional materials for biomedical applications. Chem Soc Rev 40:44–56.  https://doi.org/10.1039/b821763gCrossRefPubMedGoogle Scholar
  120. 120.
    Pekkanen AM, Mondschein RJ, Williams CB, Long TE (2017) 3D printing polymers with supramolecular functionality for biological applications. Biomacromolecules 18:2669–2687.  https://doi.org/10.1021/acs.biomac.7b00671CrossRefPubMedGoogle Scholar
  121. 121.
    Yang L, Tan X, Wang Z, Zhang X (2015) Supramolecular polymers: historical development, preparation, characterization, and functions. Chem Rev 115:7196–7239.  https://doi.org/10.1021/cr500633bCrossRefPubMedGoogle Scholar
  122. 122.
    Clarke DE, Pashuck ET, Bertazzo S, Weaver JVM, Stevens MM (2017) Self-healing, self-assembled β-sheet peptide–poly(γ-glutamic acid) hybrid hydrogels. J Am Chem Soc 139:7250–7255.  https://doi.org/10.1021/jacs.7b00528CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Bahlmann LC, Fokina A, Shoichet MS (2017) Dynamic bioengineered hydrogels as scaffolds for advanced stem cell and organoid culture. MRS Commun 7:472–486.  https://doi.org/10.1557/mrc.2017.72CrossRefGoogle Scholar
  124. 124.
    Radu-Wu LC, Yang J, Wu K, Kopeček J (2009) Self-assembled hydrogels from poly[N-(2-hydroxypropyl)methacrylamide] grafted with β-sheet peptides. Biomacromolecules 10:2319–2327.  https://doi.org/10.1021/bm9005084CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Elder AN, Dangelo NM, Kim SC, Washburn NR (2011) Conjugation of β-sheet peptides to modify the rheological properties of hyaluronic acid. Biomacromolecules 12:2610–2616.  https://doi.org/10.1021/bm200393kCrossRefPubMedGoogle Scholar
  126. 126.
    Highley CB, Rodell CB, Burdick JA (2015) Direct 3D printing of shear-thinning hydrogels into self-healing hydrogels. Adv Mater 27:5075–5079.  https://doi.org/10.1002/adma.201501234CrossRefPubMedGoogle Scholar
  127. 127.
    Li C, Faulkner-Jones A, Dun AR, Jin J, Chen P, Xing Y, Yang Z, Li Z, Shu W, Liu D, Duncan RR (2015) Rapid formation of a supramolecular polypeptide-DNA hydrogel for in situ three-dimensional multilayer bioprinting. Angew Chem Int Ed Engl 54:3957–3961.  https://doi.org/10.1002/anie.201411383CrossRefPubMedGoogle Scholar
  128. 128.
    Dubbin K, Tabet A, Heilshorn SC (2017) Quantitative criteria to benchmark new and existing bio-inks for cell compatibility. Biofabrication 9:044102.  https://doi.org/10.1088/1758-5090/aa869fCrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Wang H, Heilshorn SC (2015) Adaptable hydrogel networks with reversible linkages for tissue engineering. Adv Mater 27:3717–3736.  https://doi.org/10.1002/adma.201501558CrossRefPubMedPubMedCentralGoogle Scholar
  130. 130.
    Pashuck ET (2018) Designing self-assembling biomaterials with controlled mechanical and biological performance. In: Self-assembling biomaterials, pp 7–26.  https://doi.org/10.1016/B978-0-08-102015-9.00002-2CrossRefGoogle Scholar
  131. 131.
    Jiang Y, Chen J, Deng C, Suuronen EJ, Zhong Z (2014) Click hydrogels, microgels and nanogels: emerging platforms for drug delivery and tissue engineering. Biomaterials 35:4969–4985.  https://doi.org/10.1016/j.biomaterials.2014.03.001CrossRefPubMedGoogle Scholar
  132. 132.
    Jiang W, Li M, Chen Z, Leong KW (2016) Cell-laden microfluidic microgels for tissue regeneration. Lab Chip 16:4482–4506.  https://doi.org/10.1039/C6LC01193DCrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Griffin DR, Weaver WM, Scumpia PO, Di Carlo D, Segura T (2015) Accelerated wound healing by injectable microporous gel scaffolds assembled from annealed building blocks. Nat Mater 14:737–744. doi:  https://doi.org/10.1038/nmat4294CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Mealy JE, Chung JJ, Jeong HH, Issadore D, Lee D, Atluri P, Burdick JA (2018) Injectable granular hydrogels with multifunctional properties for biomedical applications. Adv Mater 30:1–7.  https://doi.org/10.1002/adma.201705912CrossRefGoogle Scholar

Suggested Reading

  1. Chimene D, Lennox KK, Kaunas RR, Gaharwar AK (2016) Advanced bioinks for 3D printing: a materials science perspective. Ann Biomed Eng 44(6):2090–2102CrossRefGoogle Scholar
  2. Cui H, Nowicki M, Fisher JP, Zhang LG (2017) 3D bioprinting for organ regeneration. Adv Healthc Mater 6(1).  https://doi.org/10.1002/adhm.201601118CrossRefGoogle Scholar
  3. Gopinathan J, Noh I (2018) Recent trends in bioinks for 3D printing. Biomater Res 22(1):1–15CrossRefGoogle Scholar
  4. Ji S, Guvendiren M (2017) Recent advances in bioink design for 3D bioprinting of tissues and organs. Front Bioeng Biotechnol 5:1–8CrossRefGoogle Scholar
  5. Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT (2017) The bioink: a comprehensive review on bioprintable materials. Biotechnol Adv 35(2):217–239CrossRefGoogle Scholar
  6. Jungst T, Smolan W, Schacht K, Scheibel T, Groll J (2016) Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev 116(3):1496–1539CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Paula Camacho
    • 1
  • Hafiz Busari
    • 2
  • Kelly B. Seims
    • 2
  • John W. Tolbert
    • 3
  • Lesley W. Chow
    • 1
    • 2
    Email author
  1. 1.Department of BioengineeringLehigh UniversityBethlehemUSA
  2. 2.Department of Materials Science and EngineeringLehigh UniversityBethlehemUSA
  3. 3.Department of Polymer Science and EngineeringLehigh UniversityBethlehemUSA

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