Skip to main content

Advertisement

SpringerLink
Log in

3D Bioprinting: Recent Trends and Challenges

  • Review Article
  • Published:
Journal of the Indian Institute of Science Aims and scope

Abstract

3D bioprinting is an additive biomanufacturing technology having potential to fast-forward the translational research, as it has the capability to fabricate artificial tissues and organs that closely mimic biological tissues or organs. As an emerging area of research in the field of tissue engineering, 3D bioprinting has scope in the development of implantable tissues and organs, construction of tissue/organ models and high-throughput diseased/cancer models for pharmaceutical and toxicological studies. Further, this area has diversified with the continuous upgradation of 3D bioprinters and biomaterials, which play major roles in the architectural quality and functionality of bioprinted construct. Addressing these technological complexities requires an integrated approach involving expertise from different areas of science and engineering with lateral thinking. In this review, we highlight the recent trends in 3D bioprinting of tissues and organs including recent developments in usage of material, printers and printing technologies. In addition, importance has been given to various target tissues printed using this technology with an emphasis on bioprinted tissue/cancer models.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1:
Figure 2:
Figure 3:
Figure 4:
Figure 5:

Figure illustrating sequence of steps that are followed for this technique206.

Similar content being viewed by others

References

  1. Murphy SV, Atala A (2014) 3D bioprinting of tissues and organs. Nat Biotechnol 32:773–785

    CAS  Google Scholar 

  2. Mi S, Yi X, Du Z, Xu Y, Sun W (2018) Construction of a liver sinusoid based on the laminar flow on chip and self-assembly of endothelial cells. Biofabrication 10:025010

    Google Scholar 

  3. Mazza G, Rombouts K, Rennie Hall A, Urbani L, Vinh Luong T, Al-Akkad W, Longato L, Brown D, Maghsoudlou P, Dhillon AP et al (2015) Decellularized human liver as a natural 3D-scaffold for liver bioengineering and transplantation. Sci Rep 5:13079

    CAS  Google Scholar 

  4. Baptista PM, Siddiqui MM, Lozier G, Rodriguez SR, Atala A, Soker S (2011) The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology 53:604–617

    CAS  Google Scholar 

  5. Mittal R, Woo FW, Castro CS, Cohen MA, Karanxha J, Mittal J, Chhibber T, Jhaveri VM (2019) Organ-on-chip models: implications in drug discovery and clinical applications. J Cell Physiol 234:8352–8380

    CAS  Google Scholar 

  6. 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

    CAS  Google Scholar 

  7. Guillemot F, Guillotin B, Fontaine A, Ali M, Catros S, Kériquel V, Fricain J-C, Rémy M, Bareille R, Amédée-Vilamitjana J (2011) Laser-assisted bioprinting to deal with tissue complexity in regenerative medicine. MRS Bull 36:1015–1019

    CAS  Google Scholar 

  8. Yu Y, Zhang Y, Ozbolat IT (2014) A hybrid bioprinting approach for scale-up tissue fabrication. J Manuf Sci Eng 136:061013

    Google Scholar 

  9. Chameettachal S, Sasikumar S, Sethi S, Sriya Y, Pati F (2019) Tissue/organ-derived bioink formulation for 3D bioprinting. J 3D Print Med 3:39–54

    CAS  Google Scholar 

  10. Satpathy A, Datta P, Wu Y, Ayan B, Bayram E, Ozbolat IT (2018) Developments with 3D bioprinting for novel drug discovery. Expert Opin Drug Discov 13:1115–1129

    CAS  Google Scholar 

  11. Visk DA (2015) Will advances in preclinical in vitro models lower the costs of drug development? Appl In Vitro Toxicol 1:79–82

    Google Scholar 

  12. Klebe R (1988) Cytoscribing: a method for micropositioning cells and the construction of two- and three-dimensional synthetic tissues. Exp Cell Res 179:362–373

    CAS  Google Scholar 

  13. Wilson WC, Boland T (2003) Cell and organ printing 1: protein and cell printers. Anat Rec 272A:491–496

    Google Scholar 

  14. Miller ED, Fischer GW, Weiss LE, Walker LM, Campbell PG (2006) Dose-dependent cell growth in response to concentration modulated patterns of FGF-2 printed on fibrin. Elsevier 10:2213–2221

    Google Scholar 

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

    CAS  Google Scholar 

  16. Yenilmez B, Temirel M, Knowlton S, Lepowsky E, Tasoglu S (2019) Development and characterization of a low-cost 3D bioprinter. Elsevier 13:e00044

    Google Scholar 

  17. Tuan R, Boland G, Tuli R (2003) Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5(1):32–45

    CAS  Google Scholar 

  18. Kačarević Ž, Rider P, Alkildani S, Retnasingh S, Smeets R, Jung O, Ivanišević Z, Barbeck M (2018) An introduction to 3D bioprinting: possibilities, challenges and future aspects. Materials (Basel) 6:11

    Google Scholar 

  19. Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, Huard J (2005) Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell 16:3323–3333

    CAS  Google Scholar 

  20. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, Huard J (2002) Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157(5):851–864

    CAS  Google Scholar 

  21. Rasch A (2015) Fifth congress of industrial cell technology 2014. Regen Med 10:105–107

    CAS  Google Scholar 

  22. Hewes S, Wong AD, Searson PC (2017) Bioprinting microvessels using an inkjet printer. Bioprinting 7:14–18

    Google Scholar 

  23. Cui X, Dean D, Ruggeri ZM, Boland T (2010) Cell damage evaluation of thermal inkjet printed Chinese hamster ovary cells. Biotechnol Bioeng 106:963–969

    CAS  Google Scholar 

  24. Bishop ES, Mostafa S, Pakvasa M, Luu HH, Lee MJ, Wolf JM, Lee MJ, Wolf JM, Ameer GA, He TC, Reid RR (2017) 3-D bioprinting technologies in tissue engineering and regenerative medicine: current and future trends. Genes Dis 4:185–195

    CAS  Google Scholar 

  25. Mattimore JP, Groff RE, Burg T, Pepper ME (2010) A general purpose driver board for the HP26 ink-jet cartridge with applications to bioprinting. In: Proceedings of the IEEE SoutheastCon 2010 (SoutheastCon,). pp 510–513

  26. Orloff ND, Cynthia T, Nathan C, Stephen K, Andrea H, Sean C, Victoria W, Riedel-Kruse IH (2014) Integrated bioprinting and imaging for scalable, networkable desktop experimentation. RSC Adv 4(65):34721–34728

    CAS  Google Scholar 

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

    Google Scholar 

  28. Nishiyama Y, Nakamura M, Henmi C, Yamaguchi K, Mochizuki S, Nakagawa H, Takiura K (2009) Development of a three-dimensional bioprinter: construction of cell supporting structures using hydrogel and state-of-the-art inkjet technology. J Biomech Eng 131(3):035001

    Google Scholar 

  29. Lee J-S, Hong JM, Jung JW, Shim J-H, Oh J-H, Cho D-W (2014) 3D printing of composite tissue with complex shape applied to ear regeneration. Biofabrication 6:024103

    Google Scholar 

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

    Google Scholar 

  31. Bertassoni LE, Cardoso JC, Manoharan V, Cristino AL, Bhise NS, Araujo WA, Zorlutuna P, Vrana NE, Ghaemmaghami AM, Dokmeci MR et al (2014) Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 6:024105

    Google Scholar 

  32. Ozbolat IT, Chen H, Yu Y (2014) Development of ‘Multi-arm Bioprinter’ for hybrid biofabrication of tissue engineering constructs. Robot Comput Integr Manuf 30(3):295–304

    Google Scholar 

  33. Fedorovich NE, Schuurman W, Wijnberg HM, Prins H-J, van Weeren PR, Malda J, Alblas J, Dhert WJA (2012) Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng Part C Methods 18:33–44

    CAS  Google Scholar 

  34. Fedorovich NE, Wijnberg HM, Dhert WJA, Alblas J (2011) Distinct tissue formation by heterogeneous printing of osteo- and endothelial progenitor cells. Tissue Eng Part A 17:2113–2121

    Google Scholar 

  35. Kim Y, Kang K, Yoon S, Kim JS, Park SA, Kim WD, Lee SB, Ryu K-Y, Jeong J, Choi D (2018) Prolongation of liver-specific function for primary hepatocytes maintenance in 3D printed architectures. Organogenesis 14:1–12

    CAS  Google Scholar 

  36. Jang J, Kim TG, Kim BS, Kim SW, Kwon SM, Cho DW (2016) Tailoring mechanical properties of decellularized extracellular matrix bioink by vitamin B2-induced photo-crosslinking. Acta Biomater 33:88–95

    CAS  Google Scholar 

  37. Duan B, Hockaday LA, Kang KH, Butcher JT (2013) 3D Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res Part A 101A:1255–1264

    CAS  Google Scholar 

  38. Song KH, Highley CB, Rouff A, Burdick JA (2018) Complex 3D-printed microchannels within cell-degradable hydrogels. Adv Funct Mater 28:1801331

    Google Scholar 

  39. Xu Y, Hu Y, Liu C, Yao H, Liu B, Mi S (2018) A novel strategy for creating tissue-engineered biomimetic blood vessels using 3D bioprinting technology. Materials 11(9):1581

    Google Scholar 

  40. Skardal A, Mack D, Kapetanovic E, Atala A, Jackson JD, Yoo J, Soker S (2012) Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl Med 1:792–802

    CAS  Google Scholar 

  41. 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

    CAS  Google Scholar 

  42. Mandrycky C, Wang Z, Kim K, Kim DH (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34(4):422–434

    CAS  Google Scholar 

  43. Bauwens CL, Peerani R, Niebruegge S, Woodhouse KA, Kumacheva E, Husain M, Zandstra PW (2008) Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26:2300–2310

    Google Scholar 

  44. Gaebel R, Nan M, Jun L, Jianjun G, Lothar K, Christian K, Martin G (2011) Patterning human stem cells and endothelial cells with laser printing for cardiac regeneration. Biomaterials 32(35):9218–9230

    CAS  Google Scholar 

  45. Koch L, Deiwick A, Schlie S, Michael S, Gruene M, Coger V, Zychlinski D, Schambach A, Reimers K, Vogt PM et al (2012) Skin tissue generation by laser cell printing. Biotechnol Bioeng 109:1855–1863

    CAS  Google Scholar 

  46. Gauvin R, Chen YC, Lee JW, Soman P, Zorlutuna P, Nichol JW, Bae H, Chen S, Khademhosseini A (2012) Microfabrication of complex porous tissue engineering scaffolds using 3D projection stereolithography. Biomaterials 33(15):3824–3834

    CAS  Google Scholar 

  47. Huang TQ, Qu X, Liu J, Chen S (2014) 3D printing of biomimetic microstructures for cancer cell migration. Biomed Microdevices 16:127–132

    Google Scholar 

  48. Ma X, Yu C, Wang P, Xu W, Wan X, Lai CSE, Liu J, Koroleva-Maharajh A, Chen S (2018) Rapid 3D bioprinting of decellularized extracellular matrix with regionally varied mechanical properties and biomimetic microarchitecture. Biomaterials 185:310–321

    CAS  Google Scholar 

  49. Wang Z, Abdulla R, Parker B, Samanipour R, Ghosh S, Kim K (2015) A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks. Biofabrication 7:045009

    Google Scholar 

  50. Albanna M, Binder KW, Murphy SV, Kim J, Qasem SA, Zhao W, Tan J, El-Amin IB, Dice DD, Marco J, Green J (2019) In situ bioprinting of autologous skin cells accelerates wound healing of extensive excisional full-thickness wounds. Sci Rep 9(1):1856

    Google Scholar 

  51. Binder KW, Zhao W, Aboushwareb T, Dice D, Atala A, Yoo JJ (2010) In situ bioprinting of the skin for burns. J Am Coll Surg 211(3):S76

    Google Scholar 

  52. Ding H, Chang RC (2018) Simulating image-guided in situ bioprinting of a skin graft onto a phantom burn wound bed. Addit Manuf 22:708–719

    CAS  Google Scholar 

  53. Skardal A, Murphy SV, Crowell K, Mack D, Atala A, Soker S (2017) A tunable hydrogel system for long-term release of cell-secreted cytokines and bioprinted in situ wound cell delivery. J Biomed Mater Res Part B Appl Biomater 105:1986–2000

    CAS  Google Scholar 

  54. Keriquel V, Guillemot F, Arnault I, Guillotin B, Miraux S, Amédée J, Fricain J-C, Catros S (2010) In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice. Biofabrication 2:014101

    Google Scholar 

  55. Keriquel V, Oliveira H, Rémy M, Ziane S, Delmond S, Rousseau B, Rey S, Catros S, Amédée J, Guillemot F, Fricain JC (2017) In situ printing of mesenchymal stromal cells, by laser-assisted bioprinting, for in vivo bone regeneration applications. Sci Rep 7(1):1778

    Google Scholar 

  56. Di Bella C, Duchi S, O’Connell CD, Blanchard R, Augustine C, Yue Z, Thompson F, Richards C, Beirne S, Onofrillo C et al (2018) In situ handheld three-dimensional bioprinting for cartilage regeneration. J Tissue Eng Regen Med 12:611–621

    Google Scholar 

  57. Ashammakhi N, Ahadian S, Pountos I, Hu S-K, Tellisi N, Bandaru P, Ostrovidov S, Dokmeci MR, Khademhosseini A (2019) In situ three-dimensional printing for reparative and regenerative therapy. Biomed Microdevices 21:42

    Google Scholar 

  58. Lewis PL, Green RM, Shah RN (2018) 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater 69:63–70

    CAS  Google Scholar 

  59. Wang X, Yan Y, Pan Y, Xiong Z, Liu H, Cheng J, Liu F, Lin F, Wu R, Zhang R et al (2006) Generation of three-dimensional hepatocyte/gelatin structures with rapid prototyping system. Tissue Eng 12:83–90

    CAS  Google Scholar 

  60. Ahn SH, Lee HJ, Lee JS, Yoon H, Chun W, Kim GH (2015) A novel cell-printing method and its application to hepatogenic differentiation of human adipose stem cell-embedded mesh structures. Sci Rep 5:13427

    CAS  Google Scholar 

  61. You F, Wu X, Zhu N, Lei M, Eames BF, Chen X (2016) 3D printing of porous cell-laden hydrogel constructs for potential applications in cartilage tissue engineering. ACS Biomater Sci Eng 2:1200–1210

    CAS  Google Scholar 

  62. Xiong R, Zhang Z, Chai W, Huang Y, Chrisey DB (2015) Freeform drop-on-demand laser printing of 3D alginate and cellular constructs. Biofabrication 7:045011

    Google Scholar 

  63. Yoon H, Lee J, Yim H, Kim G (2016) Development of cell-laden 3D scaffolds for efficient engineered skin substitutes by collagen gelation. RSC Adv 6:21439–21447

    CAS  Google Scholar 

  64. Lee W, Debasitis J, Lee V, Lee J (2009) Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials 30(8):1587–1595

    CAS  Google Scholar 

  65. Schacht K, Jüngst T, Schweinlin M, Ewald A, Groll J, Scheibel T (2015) Biofabrication of cell-loaded 3D Spider silk constructs. Angew Chemie Int Ed 54:2816–2820

    CAS  Google Scholar 

  66. Das S, Pati F, Choi Y, Rijal G, Shim J (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

    CAS  Google Scholar 

  67. Rodriguez M, Brown J, Giordano J (2017) Silk based bioinks for soft tissue reconstruction using 3-dimensional (3D) printing with in vitro and in vivo assessments. Biomaterials 117:105–115

    CAS  Google Scholar 

  68. Wu Z, Su X, Xu Y, Kong B, Sun W (2016) Bioprinting three-dimensional cell-laden tissue constructs with controllable degradation. Sci Rep 6:24474

    CAS  Google Scholar 

  69. Lee HJ, Kim YB, Ahn SH, Lee J-S, Jang CH, Yoon H, Chun W, Kim GH (2015) A new approach for fabricating collagen/ECM-based bioinks using preosteoblasts and human adipose stem cells. Adv Healthc Mater 4:1359–1368

    CAS  Google Scholar 

  70. Elomaa L, Pan C, Shanjani Y (2015) Three-dimensional fabrication of cell-laden biodegradable poly (ethylene glycol-co-depsipeptide) hydrogels by visible light stereolithography. J Mater Chem B 3(42):8348–8358

    CAS  Google Scholar 

  71. Shim J-H, Kim JY, Park M, Park J, Cho D-W (2011) Development of a hybrid scaffold with synthetic biomaterials and hydrogel using solid freeform fabrication technology. Biofabrication 3:034102

    Google Scholar 

  72. Datta P, Barui A, Wu Y, Ozbolat V, Moncal KK, Ozbolat IT (2018) Essential steps in bioprinting: from pre- to post-bioprinting. Biotechnol Adv 36:1481–1504

    CAS  Google Scholar 

  73. Jia J, Richards D, Pollard S, Tan Y (2014) Engineering alginate as bioink for bioprinting. Acta Biomater 10(10):4323–4331

    CAS  Google Scholar 

  74. Kesti M, Eberhardt C, Pagliccia G, Kenkel D, Grande D, Boss A, Zenobi-Wong M (2015) Bioprinting complex cartilaginous structures with clinically compliant biomaterials. Adv Funct Mater 25:7406–7417

    Google Scholar 

  75. Yeo M, Lee J-S, Chun W, Kim GH (2016) An innovative collagen-based cell-printing method for obtaining human adipose stem cell-laden structures consisting of core-sheath structures for tissue engineering. Biomacromolecules 17:1365–1375

    CAS  Google Scholar 

  76. Gu Q, Tomaskovic-Crook E, Lozano R, Chen Y, Kapsa RM, Zhou Q, Wallace GG, Crook JM (2016) Functional 3D neural mini-tissues from printed gel-based bioink and human neural stem cells. Adv Healthc Mater 5:1429–1438

    CAS  Google Scholar 

  77. Daly AC, Cunniffe GM, Sathy BN, Jeon O, Alsberg E, Kelly DJ (2016) 3D bioprinting of developmentally inspired templates for whole bone organ engineering. Adv Healthc Mater 5:2353–2362

    CAS  Google Scholar 

  78. Kim Y, Lee H, Yang G, Choi C (2016) Mechanically reinforced cell-laden scaffolds formed using alginate-based bioink printed onto the surface of a PCL/alginate mesh structure for regeneration of hard tissue. J Colloid Interface Sci 461:359–368

    CAS  Google Scholar 

  79. Merceron TK, Burt M, Seol Y-J, Kang H-W, Lee SJ, Yoo JJ, Atala A (2015) A 3D bioprinted complex structure for engineering the muscle-tendon unit. Biofabrication 7:035003

    Google Scholar 

  80. Saberianpour S, Heidarzadeh M, Geranmayeh MH, Hosseinkhani H, Rahbarghazi R, Nouri M (2018) Tissue engineering strategies for the induction of angiogenesis using biomaterials. J Biol Eng 12:36

    CAS  Google Scholar 

  81. Laschke M (2012) Vascularization in tissue engineering: angiogenesis versus inosculation. Eur Surg Res 48(2):85–92

    CAS  Google Scholar 

  82. Lee J, Choi Y, Yong W, Pati F (2016) Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication 8(1):015007

    Google Scholar 

  83. Colosi C, Shin SR, Manoharan V, Massa S, Costantini M, Barbetta A, Dokmeci MR, Dentini M, Khademhosseini A (2016) Microfluidic bioprinting of heterogeneous 3D tissue constructs using low-viscosity bioink. Adv Mater 28:677–684

    CAS  Google Scholar 

  84. Cooper GM, Miller ED, Decesare GE, Usas A, Lensie EL, Bykowski MR, Huard J, Weiss LE, Losee JE, Campbell PG (2010) Inkjet-based biopatterning of bone morphogenetic protein-2 to spatially control calvarial bone formation. Tissue Eng Part A 16:1749–1759

    CAS  Google Scholar 

  85. Chiu LL, Radisic M (2010) Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues. Biomaterials 31(2):226–241

    CAS  Google Scholar 

  86. Zhu W, Cui H, Boualam B, Masood F, Flynn E, Rao RD, Zhang ZY, Zhang LG (2018) 3D bioprinting mesenchymal stem cell-laden construct with core–shell nanospheres for cartilage tissue engineering. Nanotechnology 29(18):185101

    Google Scholar 

  87. Gruene M, Pflaum M, Deiwick A, Koch L, Schlie S, Unger C, Wilhelmi M, Haverich A, Chichkov BN (2011) Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3:015005

    CAS  Google Scholar 

  88. Jamróz W, Szafraniec J, Kurek M, Jachowicz R (2018) 3D printing in pharmaceutical and medical applications, recent achievements and challenges. Pharm Res 35:176

    Google Scholar 

  89. Kim J, Seol Y, Ko I, Kang H, Lee Y (2018) 3D bioprinted human skeletal muscle constructs for muscle function restoration. Sci Rep 8(1):12307

    Google Scholar 

  90. Vanderburgh J, Sterling JA, Guelcher SA (2017) 3D printing of tissue engineered constructs for in vitro modeling of disease progression and drug screening. Ann Biomed Eng 45:164–179

    Google Scholar 

  91. Mestre R, Patiño T, Barceló X, Anand S, Pérez-Jiménez A, Sánchez S (2018) Force modulation and adaptability of 3D-bioprinted biological actuators based on skeletal muscle tissue. Adv Mater Technol 4:1800631

    Google Scholar 

  92. Powell CA, Smiley BL, Mills J, Vandenburgh HH (2002) Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Physiol Physiol 283:C1557–C1565

    CAS  Google Scholar 

  93. Kang H, Lee S, Ko I, Kengla C, Yoo JJ, Atala A (2016) undefined: a 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 3:312–319

    Google Scholar 

  94. Mozetic P, Giannitelli SM, Gori M, Trombetta M, Rainer A (2017) Engineering muscle cell alignment through 3D bioprinting. J Biomed Mater Res Part A 105:2582–2588

    CAS  Google Scholar 

  95. Yeo M, Lee H, Kim GH (2016) Combining a micro/nano-hierarchical scaffold with cell-printing of myoblasts induces cell alignment and differentiation favorable to skeletal muscle tissue regeneration. Biofabrication 8:035021

    Google Scholar 

  96. Yeo M, Kim G (2018) Three-dimensional microfibrous bundle structure fabricated using an electric field-assisted/cell printing process for muscle tissue regeneration. ACS Biomater Sci Eng 4:728–738

    CAS  Google Scholar 

  97. Cui X, Gao G, Qiu Y (2013) Accelerated myotube formation using bioprinting technology for biosensor applications. Biotechnol Lett 35:315–321

    CAS  Google Scholar 

  98. Choi Y-J, Kim TG, Jeong J, Yi H-G, Park JW, Hwang W, Cho D-W (2016) 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink. Adv Healthc Mater 5:2636–2645

    CAS  Google Scholar 

  99. Moore CA, Shah NN, Smith CP, Rameshwar P (2018) 3D bioprinting and stem cells. Somat Stem Cells 1842:93–103

    CAS  Google Scholar 

  100. Allen JW, Bhatia SN (2002) Engineering liver therapies for the future. Tissue Eng 8:725–737

    CAS  Google Scholar 

  101. Mazza G, Al-Akkad W, Rombouts K, Pinzani M (2018) Liver tissue engineering: from implantable tissue to whole organ engineering. Hepatol Commun 2:131–141

    Google Scholar 

  102. Ware BR, Khetani SR (2017) Engineered liver platforms for different phases of drug development. Trends Biotechnol 35(2):172–183

    CAS  Google Scholar 

  103. Du Y, Li N, Yang H, Luo C, Gong Y, Tong C, Gao Y, Lü S, Long M (2017) Mimicking liver sinusoidal structures and functions using a 3D-configured microfluidic chip. Lab Chip 17(5):782–794

    CAS  Google Scholar 

  104. LeCluyse EL, Witek RP, Andersen ME, Powers MJ (2012) Organotypic liver culture models: meeting current challenges in toxicity testing. Crit Rev Toxicol 42:501–548

    CAS  Google Scholar 

  105. Retting K, Carter D, Crogan-Grundy C, Khatiwala C, Norona L, Paffenroth E, Hanumegowda U, Chen A, Hazelwood L, Lehman-McKeeman L et al (2018) Modeling liver biology and the tissue response to injury in bioprinted human liver tissues. Appl In Vitro Toxicol 4:288–303

    CAS  Google Scholar 

  106. Nguyen DG, Funk J, Robbins JB, Crogan-Grundy C, Presnell SC, Singer T, Roth AB (2016) Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS One 11:e0158674

    Google Scholar 

  107. Lee H, Cho DW (2016) One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3D bioprinting technology. Lab Chip 16(14):2618–2625

    CAS  Google Scholar 

  108. Norotte C, Marga FS, Niklason LE, Forgacs G (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30(30):5910–5917

    CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  111. Lazar A, Mann HJ, Remmel RP, Shatford RA, Cerra FB, Hu W-S (1995) Extended liver-specific functions of porcine hepatocyte spheroids entrapped in collagen gel. In Vitro Cell Dev Biol Anim 31:340–346

    CAS  Google Scholar 

  112. Kizawa H, Nagao E, Shimamura M, Zhang G, Torii H (2017) Scaffold-free 3D bio-printed human liver tissue stably maintains metabolic functions useful for drug discovery. Biochem Biophys Rep 10:186–191

    Google Scholar 

  113. Astashkina AI, Mann BK, Prestwich GD, Grainger DW (2012) Comparing predictive drug nephrotoxicity biomarkers in kidney 3-D primary organoid culture and immortalized cell lines. Biomaterials 33(18):4712–4721

    CAS  Google Scholar 

  114. King SM, Higgins JW, Nino CR, Smith TR, Paffenroth EH, Fairbairn CE, Docuyanan A, Shah VD, Chen AE, Presnell SC et al (2017) 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol 8:123

    Google Scholar 

  115. Homan KA, Kolesky DB, Skylar-Scott MA, Herrmann J, Obuobi H, Moisan A, Lewis JA (2016) Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep 6:34845

    CAS  Google Scholar 

  116. De la Vega L, Rosas Gómez DA, Abelseth E, Abelseth L, Allisson da Silva V, Willerth S (2018) 3D bioprinting human induced pluripotent stem cell-derived neural tissues using a novel lab-on-a-printer technology. Appl Sci 8(12):2414

    Google Scholar 

  117. Joung D, Truong V, Neitzke CC, Guo S-Z, Walsh PJ, Monat JR, Meng F, Park SH, Dutton JR, Parr AM et al (2018) 3D printed stem-cell derived neural progenitors generate spinal cord scaffolds. Adv Funct Mater 28:1801850

    Google Scholar 

  118. Li X, Wang X, Wang X, Chen H, Zhang X, Zhou L, Xu T (2018) 3D bioprinted rat Schwann cell-laden structures with shape flexibility and enhanced nerve growth factor expression. 3 Biotech 8:342

    Google Scholar 

  119. Lee W, Pinckney J, Lee V, Lee JH, Fischer K, Polio S, Park JK, Yoo SS (2009) Three-dimensional bioprinting of rat embryonic neural cells. Neuroreport 20(8):798–803

    Google Scholar 

  120. Ashammakhi N, Hasan A, Kaarela O, Byambaa B, Sheikhi A, Gaharwar AK, Khademhosseini A (2019) Advancing frontiers in bone bioprinting. Adv Healthc Mater 8:1801048

    Google Scholar 

  121. Zhang YS, Khademhosseini A (2017) Advances in engineering hydrogels. Science 356:eaaf3627

    Google Scholar 

  122. Duarte Campos DF, Blaeser A, Buellesbach K, Sen KS, Xun W, Tillmann W, Fischer H (2016) Bioprinting organotypic hydrogels with improved mesenchymal stem cell remodeling and mineralization properties for bone tissue engineering. Adv Healthc Mater 5:1336–1345

    CAS  Google Scholar 

  123. Raja N, Yun HS (2016) A simultaneous 3D printing process for the fabrication of bioceramic and cell-laden hydrogel core/shell scaffolds with potential application in bone tissue regeneration. J Mater Chem B 4(27):4707–4716

    CAS  Google Scholar 

  124. Kim WJ, Yun H-S, Kim GH (2017) An innovative cell-laden α-TCP/collagen scaffold fabricated using a two-step printing process for potential application in regenerating hard tissues. Sci Rep 7:3181

    Google Scholar 

  125. O’Connell CD, Di Bella C, Thompson F, Augustine C, Beirne S, Cornock R, Richards CJ, Chung J, Gambhir S, Yue Z et al (2016) Development of the Biopen: a handheld device for surgical printing of adipose stem cells at a chondral wound site. Biofabrication 8:015019

    Google Scholar 

  126. 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:e0177628

    Google Scholar 

  127. Cui H, Zhu W, Nowicki M, Zhou X, Khademhosseini A, Zhang LG (2016) Hierarchical fabrication of engineered vascularized bone biphasic constructs via dual 3D bioprinting: integrating regional bioactive factors into architectural design. Adv Healthc Mater 5:2174–2181

    CAS  Google Scholar 

  128. Bendtsen ST, Quinnell SP, Wei M (2017) Development of a novel alginate-polyvinyl alcohol-hydroxyapatite hydrogel for 3D bioprinting bone tissue engineered scaffolds. J Biomed Mater Res A 105:1457–1468

    CAS  Google Scholar 

  129. Byambaa B, Annabi N, Yue K, Trujillo-de Santiago G, Alvarez MM, Jia W, Kazemzadeh-Narbat M, Shin SR, Tamayol A, Khademhosseini A (2017) Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv Healthc Mater 6:1700015

    Google Scholar 

  130. Demirtaş TT, Irmak G, Gümüşderelioğlu M (2017) A bioprintable form of chitosan hydrogel for bone tissue engineering. Biofabrication 9(3):035003

    Google Scholar 

  131. Sophia Fox AJ, Bedi A, Rodeo SA (2009) The basic science of articular cartilage: structure, composition, and function. Sport Health A Multidiscip Approach 1:461–468

    Google Scholar 

  132. Kimlin Lauren C, Casagrande Giovanna, Virador Victoria M (2013) In vitro three-dimensional (3D) models in cancer research: an update. Mol Carcinog 52(3):167–182

    Google Scholar 

  133. Olubamiji AD, Zhu N, Chang T, Nwankwo CK, Izadifar Z, Honaramooz A, Chen X, Eames BF (2017) Traditional invasive and synchrotron-based noninvasive assessments of three-dimensional-printed hybrid cartilage constructs in situ. Tissue Eng Part C Methods 23:156–168

    Google Scholar 

  134. Gao G, Zhang X-F, Hubbell K, Cui X (2017) NR2F2 regulates chondrogenesis of human mesenchymal stem cells in bioprinted cartilage. Biotechnol Bioeng 114:208–216

    CAS  Google Scholar 

  135. 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

    CAS  Google Scholar 

  136. 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

    CAS  Google Scholar 

  137. Nguyen D, Hägg DA, Forsman A, Ekholm J, Nimkingratana P, Brantsing C, Kalogeropoulos T, Zaunz S, Concaro S, Brittberg M et al (2017) Cartilage tissue engineering by the 3D Bioprinting of iPS cells in a nanocellulose/alginate bioink. Sci Rep 7:658

    Google Scholar 

  138. Apelgren P, Karabulut E, Amoroso M, Mantas A, Martínez Ávila H, Kölby L, Kondo T, Toriz G, Gatenholm P (2019) In vivo human cartilage formation in three-dimensional bioprinted constructs with a novel bacterial nanocellulose bioink. ACS Biomater Sci Eng 5:2482–2490

    CAS  Google Scholar 

  139. Wang Z, Lee SJ, Cheng HJ, Yoo JJ, Atala A (2018) 3D bioprinted functional and contractile cardiac tissue constructs. Acta Biomater 70:48–56

    CAS  Google Scholar 

  140. Pomeroy JE, Helfer A, Bursac N (2019) Biomaterializing the promise of cardiac tissue engineering. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2019.02.009

    Article  Google Scholar 

  141. Liu J, He J, Liu J, Ma X, Chen Q, Lawrence N, Zhu W, Xu Y, Chen S (2019) Rapid 3D bioprinting of in vitro cardiac tissue models using human embryonic stem cell-derived cardiomyocytes. J Bprint 13:e00040

    Google Scholar 

  142. See F, Kompa A, Martin J, Lewis DA, Krum H (2005) Fibrosis as a therapeutic target post-myocardial infarction. Curr Pharm Des 11(4):477–487

    CAS  Google Scholar 

  143. Lee VK, Kim DY, Ngo H, Lee Y, Seo L, Yoo SS, Dai G (2014) Creating perfused functional vascular channels using 3D bio-printing technology. Biomaterials 35(28):8092–8102

    CAS  Google Scholar 

  144. Maiullari F, Costantini M, Milan M, Pace V, Chirivì M, Maiullari S, Gargioli C (2018) A multi-cellular 3D bioprinting approach for vascularized heart tissue engineering based on HUVECs and iPSC-derived cardiomyocytes. Sci Rep 8(1):13532

    Google Scholar 

  145. Liu J, He J, Liu J, Ma X, Chen Q, Lawrence N, Chen S (2019) Rapid 3D bioprinting of in vitro cardiac tissue models using human embryonic stem cell-derived cardiomyocytes. Bioprinting 13:e00040

    Google Scholar 

  146. Coderch L, Lpez O, de la Maza A, Parra JL (2003) Ceramides and skin function. Am J Clin Dermatol 4:107–129

    Google Scholar 

  147. Zhong SP, Zhang YZ, Lim CT (2010) Tissue scaffolds for skin wound healing and dermal reconstruction. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:510–525

    CAS  Google Scholar 

  148. Rahmani Del Bakhshayesh A, Annabi N, Khalilov R, Akbarzadeh A, Samiei M, Alizadeh E, Alizadeh-Ghodsi M, Davaran S, Montaseri A (2018) Recent advances on biomedical applications of scaffolds in wound healing and dermal tissue engineering. Artif Cells Nanomed Biotechnol 46:691–705

    CAS  Google Scholar 

  149. Navarro FA, Stoner ML, Park CS, Huertas JC, Lee HB, Wood FM, Orgill DP (2000) Sprayed keratinocyte suspensions accelerate epidermal coverage in a porcine microwound model. J Burn Care Rehabilit 21(6):513–518

    CAS  Google Scholar 

  150. ter Horst B, Chouhan G, Moiemen NS, Grover LM (2018) Advances in keratinocyte delivery in burn wound care. Adv Drug Deliv Rev 123:18–32

    Google Scholar 

  151. Vasconcelos A, Gomes AC, Cavaco-Paulo A (2012) Novel silk fibroin/elastin wound dressings. Acta Biomater 8(8):3049–3060

    CAS  Google Scholar 

  152. Prunieras M, Regnier M, Woodley D (1983) Methods for cultivation of keratinocytes with an air–liquid interface. J Investig Dermatol 81(1):S28–S33

    Google Scholar 

  153. Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, Yoo S-S, Dai G, Karande P (2014) Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods 20:473–484

    CAS  Google Scholar 

  154. Cubo N, Garcia M, del Cañizo JF, Velasco D, Jorcano JL (2016) 3D bioprinting of functional human skin: production and in vivo analysis. Biofabrication 9:015006

    Google Scholar 

  155. Zhang L, Fisher J, Leong K (2015) 3D bioprinting and nanotechnology in tissue engineering and regenerative medicine. Academic Press, Cambridge

    Google Scholar 

  156. Leong MF, Toh JKC, Du C, Narayanan K, Lu HF, Lim TC, Wan ACA, Ying JY (2013) Patterned prevascularised tissue constructs by assembly of polyelectrolyte hydrogel fibres. Nat Commun 4:2353

    Google Scholar 

  157. Ko HC, Milthorpe BK, McFarland CD (2017) Engineering thick tissues-the vascularisation problem. Eur Cells Mater 14:1–19

    Google Scholar 

  158. Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, Mackem S, Carmeliet G, Kronenberg HM (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19:329–344

    CAS  Google Scholar 

  159. Reinert RB, Cai Q, Hong JY, Plank JL, Aamodt K, Prasad N, Labosky PA (2014) Vascular endothelial growth factor coordinates islet innervation via vascular scaffolding. Development 141(7):1480–1491

    CAS  Google Scholar 

  160. Criswell TL, Corona BT, Wang Z, Zhou Y, Niu G, Xu Y, Soker S (2013) The role of endothelial cells in myofiber differentiation and the vascularization and innervation of bioengineered muscle tissue in vivo. Biomaterials 34(1):140–149

    CAS  Google Scholar 

  161. Gálvez-Montón C, Fernandez-Figueras MT, Martí M, Soler-Botija C, Roura S, Perea-Gil I, Prat-Vidal C, Llucià-Valldeperas A, Raya Á, Bayes-Genis A (2015) Neoinnervation and neovascularization of acellular pericardial-derived scaffolds in myocardial infarcts. Stem Cell Res Ther 6:108

    Google Scholar 

  162. Hatch J, Mukouyama Y (2015) Spatiotemporal mapping of vascularization and innervation in the fetal murine intestine. Dev Dyn 244:56–68

    Google Scholar 

  163. Datta P, Ayan B, Ozbolat IT (2017) Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater 51:1–20

    CAS  Google Scholar 

  164. Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA (2016) Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci 113(12):3179–3184

    CAS  Google Scholar 

  165. Gao G, Lee JH, Jang J, Lee DH, Kong J-S, Kim BS, Choi Y-J, Jang WB, Hong YJ, Kwon S-M et al (2017) Tissue engineered bio-blood-vessels constructed using a tissue-specific bioink and 3D coaxial cell printing technique: a novel therapy for ischemic disease. Adv Funct Mater 27:1700798

    Google Scholar 

  166. Schöneberg J, De Lorenzi F, Theek B, Blaeser A, Rommel D, Kuehne AJ, Fischer H (2018) Engineering biofunctional in vitro vessel models using a multilayer bioprinting technique. Sci Rep 8(1):10430

    Google Scholar 

  167. Bertassoni LE, Cecconi M, Manoharan V, Nikkhah M, Hjortnaes J, Cristino AL, Khademhosseini A (2014) Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab on a Chip 14(13):2202–2211

    CAS  Google Scholar 

  168. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen DHT, Cohen DM, Chaturvedi R (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11(9):768

    CAS  Google Scholar 

  169. Zhu W, Qu X, Zhu J, Ma X, Patel S, Liu J, Wang P, Lai CSE, Gou M, Xu Y et al (2017) Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials 124:106–115

    CAS  Google Scholar 

  170. Xu Y, Hu Y, Liu C, Yao H, Liu B, Mi S (2018) A novel strategy for creating tissue-engineered biomimetic blood vessels using 3D bioprinting technology. Materials (Basel) 11:158

    Google Scholar 

  171. Miller AJ, Spence JR (2017) In vitro models to study human lung development. Dis Homeost Physiol 32:246–260

    CAS  Google Scholar 

  172. Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Vacanti JP (2010) Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 16(8):927

    CAS  Google Scholar 

  173. Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, Raredon MB, Herzog E (2010) Tissue-engineered lungs for in vivo implantation. Science 329(5991):538–541

    CAS  Google Scholar 

  174. Moroni L, Burdick JA, Highley C, Lee SJ, Morimoto Y, Takeuchi S, Yoo JJ (2018) Biofabrication strategies for 3D in vitro models and regenerative medicine. Nat Rev Mater 3(5):21

    CAS  Google Scholar 

  175. Horváth L, Umehara Y, Jud C, Blank F, Petri-Fink A, Rothen-Rutishauser B (2015) Engineering an in vitro air-blood barrier by 3D bioprinting. Sci Rep 5:7974

    Google Scholar 

  176. Poomathi N, Singh S, Prakash C, Patil RV, Perumal PT, Barathi VA, Balasubramanian KK, Ramakrishna S, Maheshwari NU (2019) Bioprinting in ophthalmology: current advances and future pathways. Rapid Prototyp J 25:496–514

    Google Scholar 

  177. Srikumaran D, Munoz B, Aldave AJ, Aquavella JV, Hannush SB, Schultze R, Akpek EK (2014) Long-term outcomes of Boston type 1 keratoprosthesis implantation: a retrospective multicenter cohort. Ophthalmology 121(11):2159–2164

    Google Scholar 

  178. Crawford GJ (2016) The development and results of an artificial cornea: AlphaCor™. In: Biomaterials and regenerative medicine in ophthalmology. Woodhead Publishing, pp 443–462

  179. Sommer AC, Blumenthal EZ (2019) Implementations of 3D printing in ophthalmology. Graefe’s Arch Clin Exp Ophthalmol. https://doi.org/10.1007/s00417-019-04312-3

    Article  Google Scholar 

  180. Duarte Campos DF, Rohde M, Ross M, Anvari P, Blaeser A, Vogt M, Panfil C, Yam GH, Mehta JS, Fischer H et al (2019) Corneal bioprinting utilizing collagen-based bioinks and primary human keratocytes. J Biomed Mater Res Part A 107:1945–1953

    CAS  Google Scholar 

  181. Kim H, Jang J, Park J, Lee KP, Lee S, Lee DM, Cho DW (2019) Shear-induced alignment of collagen fibrils using 3D cell printing for corneal stroma tissue engineering. Biofabrication 11(3):035017

    Google Scholar 

  182. Miotto M, Gouveia RM, Ionescu AM, Figueiredo F, Hamley IW, Connon CJ (2019) 4D corneal tissue engineering: achieving time-dependent tissue self-curvature through localized control of cell actuators. Adv Funct Mater 29:1807334

    Google Scholar 

  183. Junttila MR, de Sauvage FJ (2013) Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501(7467):346

    CAS  Google Scholar 

  184. Cavo M, Fato M, Peñuela L, Beltrame F, Raiteri R, Scaglione S (2016) Microenvironment complexity and matrix stiffness regulate breast cancer cell activity in a 3D in vitro model. Sci Rep 6:35367

    CAS  Google Scholar 

  185. Puls TJ, Tan X, Husain M, Whittington CF, Fishel ML, Voytik-Harbin SL (2018) Development of a novel 3D tumor-tissue invasion model for high-throughput, high-content phenotypic drug screening. Sci Rep 8(1):13039

    CAS  Google Scholar 

  186. Mironov V, Trusk T, Kasyanov V, Little S, Swaja R, Markwald R (2009) Biofabrication: a 21st century manufacturing paradigm. Biofabrication 1(2):022001

    CAS  Google Scholar 

  187. Kim JB (2005) Three-dimensional tissue culture models in cancer biology. Semin Cancer Biol 15(5):365–377

    Google Scholar 

  188. Lee GY, Kenny PA, Lee EH, Bissell MJ (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4(4):359

    CAS  Google Scholar 

  189. Bissell MJ, Radisky D (2001) Putting tumours in context. Nat Rev Cancer 1(1):46

    CAS  Google Scholar 

  190. Nyga A, Cheema U, Loizidou M (2011) 3D tumour models: novel in vitro approaches to cancer studies. J Cell Commun Signal 5(3):239

    Google Scholar 

  191. Zanoni M, Piccinini F, Arienti C, Zamagni A, Santi S, Polico R, Tesei A (2016) 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci Rep 6:19103

    CAS  Google Scholar 

  192. Vargo-Gogola T, Rosen JM (2007) Modelling breast cancer: one size does not fit all. Nat Rev Cancer 7(9):659

    CAS  Google Scholar 

  193. Schwartz MA, Chen CS (2013) Deconstructing dimensionality. Science 339(6118):402–404

    CAS  Google Scholar 

  194. Kunz-Schughart LA (1999) Multicellular tumor spheroids: intermediates between monolayer culture and in vivo tumor. Cell Biol Int 23(3):157–161

    CAS  Google Scholar 

  195. Kim JW, Ho WJ, Wu BM (2011) The role of the 3D environment in hypoxia-induced drug and apoptosis resistance. Anticancer Res 31(10):3237–3245

    CAS  Google Scholar 

  196. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 148(1):3–15

    CAS  Google Scholar 

  197. Fukumura D, Jain RK (2007) Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 101:937–949

    CAS  Google Scholar 

  198. Zhao Y, Yao R, Ouyang L, Ding H, Zhang T, Zhang K, Cheng S, Sun W (2014) Three-dimensional printing of Hela cells for cervical tumor model in vitro. Biofabrication 6:035001

    Google Scholar 

  199. Chopra V, Dinh TV, Hannigan EV (1997) Three-dimensional endothelial-tumor epithelial cell interactions in human cervical cancers. In Vitro Cell Dev Biol Anim 33:432–442

    CAS  Google Scholar 

  200. Ridky TW, Chow JM, Wong DJ, Khavari PA (2010) Invasive three-dimensional organotypic neoplasia from multiple normal human epithelia. Nat Med 16:1450–1455

    CAS  Google Scholar 

  201. Herter-Sprie GS, Kung AL, Wong K-K (2013) New cast for a new era: preclinical cancer drug development revisited. J Clin Investig 123:3639–3645

    CAS  Google Scholar 

  202. Zhu W, Castro NJ, Cui H, Zhou X, Boualam B, McGrane R, Glazer RI, Zhang LG (2016) A 3D printed nano bone matrix for characterization of breast cancer cell and osteoblast interactions. Nanotechnology 27:315103

    Google Scholar 

  203. Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, Polverini PJ, Mooney DJ (2007) Engineering tumors with 3D scaffolds. Nat Methods 4:855–860

    CAS  Google Scholar 

  204. Yi HG, Jeong YH, Kim Y, Choi YJ, Moon HE, Park SH, Paek SH (2019) A bioprinted human-glioblastoma-on-a-chip for the identification of patient-specific responses to chemoradiotherapy. Nat Biomed Eng 3:509–519

    CAS  Google Scholar 

  205. Zhu W, Holmes B, Glazer RI, Zhang LG (2016) 3D printed nanocomposite matrix for the study of breast cancer bone metastasis. Nanomed Nanotechnol Biol Med 12:69–79

    CAS  Google Scholar 

  206. Miller Jordan S, Stevens Kelly R, Yang Michael T, Baker Brendon M, Nguyen Duc-Huy T, Cohen Daniel M, Toro Esteban, Chen Alice A, Galie Peter A, Xiang Yu, Chaturvedi Ritika, Bhatia Sangeeta N, Chen Christopher S (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11:768–774

    CAS  Google Scholar 

  207. Wang Y, Mirza S, Wu S, Zeng J, Shi W, Band H, Band V, Duan B (2018) 3D hydrogel breast cancer models for studying the effects of hypoxia on epithelial to mesenchymal transition. Oncotarget 9:32191–32203

    Google Scholar 

  208. Dababneh AB, Ozbolat IT (2014) Bioprinting technology: a current state-of-the-art review. J Manuf Sci Eng 136:061016

    Google Scholar 

  209. Nagy JA, Chang S-H, Dvorak AM, Dvorak HF (2009) Why are tumour blood vessels abnormal and why is it important to know? Br J Cancer 100:865–869

    CAS  Google Scholar 

  210. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP, Jain RK (1998) Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci 95:4607–4612

    CAS  Google Scholar 

  211. Dickinson LE, Lütgebaucks C, Lewis DM, Gerecht S (2012) Patterning microscale extracellular matrices to study endothelial and cancer cell interactions in vitro. Lab Chip 12:4244

    CAS  Google Scholar 

  212. Baish JW, Stylianopoulos T, Lanning RM, Kamoun WS, Fukumura D, Munn LL, Jain RK (2011) Scaling rules for diffusive drug delivery in tumor and normal tissues. Proc Natl Acad Sci 2(108):1799–1803

    Google Scholar 

  213. Chauhan VP, Stylianopoulos T, Martin JD, Popović Z, Chen O, Kamoun WS, Bawendi MG, Fukumura D, Jain RK (2012) Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat Nanotechnol 7:383–388

    CAS  Google Scholar 

  214. Unger C, Kramer N, Walzl A, Scherzer M, Hengstschläger M, Dolznig H (2014) Modeling human carcinomas: physiologically relevant 3D models to improve anti-cancer drug development. Adv Drug Deliv Rev 79–80:50–67

    Google Scholar 

  215. Paxton N, Smolan W, Böck T, Melchels F, Groll J, Jungst T (2017) Proposal to assess printability of bioinks for extrusion-based bioprinting and evaluation of rheological properties governing bioprintability. Biofabrication 9:044107

    Google Scholar 

  216. Patra S, Young V (2016) A Review of 3D Printing Techniques and the Future in Biofabrication of Bioprinted Tissue. Cell Biochem Biophys 74:93–98

    CAS  Google Scholar 

  217. Malkoc V (2018) Challenges and the future of 3D bioprinting. J Biomed Imaging Bioeng 2(1):64–65

    Google Scholar 

  218. Letourneau CA, Davies CT, Tabibkhoei F, Daubert GL, Beck JM, Schryber JW, Quinn TZ (2015) 3D printing of medical devices: when a novel technology meets traditional legal principles. Reed Smith

  219. Gillette BM, Jensen JA, Wang M, Tchao J, Sia SK (2010) Dynamic hydrogels: switching of 3D microenvironments using two-component naturally derived extracellular matrices. Adv Mater 22:686–691

    CAS  Google Scholar 

  220. Harrison BS, Eberli D, Lee SJ, Atala A, Yoo JJ (2007) Oxygen producing biomaterials for tissue regeneration. Biomaterials 28:4628–4634

    CAS  Google Scholar 

  221. Lee W, Lee V, Polio S, Keegan P, Lee J-H, Fischer K, Park J-K, Yoo S-S (2010) On-demand three-dimensional freeform fabrication of multi-layered hydrogel scaffold with fluidic channels. Biotechnol Bioeng. https://doi.org/10.1002/bit.22613

    Article  Google Scholar 

  222. Ye K, Felimban R, Traianedes K, Moulton SE, Wallace GG, Chung J, Quigley A, Choong PFM, Myers DE (2014) Chondrogenesis of infrapatellar fat pad derived adipose stem cells in 3D printed chitosan scaffold. PLoS One 9:e99410

    Google Scholar 

  223. Poldervaart MT, Wang H, van der Stok J, Weinans H, Leeuwenburgh SCG, Öner FC, Dhert WJA, Alblas J (2013) Sustained release of BMP-2 in bioprinted alginate for osteogenicity in mice and rats. PLoS One 8:e72610

    CAS  Google Scholar 

  224. Duarte Campos DF, Blaeser A, Korsten A, Neuss S, Jäkel J, Vogt M, Fischer H (2015) The stiffness and structure of three-dimensional printed hydrogels direct the differentiation of mesenchymal stromal cells toward adipogenic and osteogenic lineages. Tissue Eng Part A 21:740–756

    CAS  Google Scholar 

  225. Xu T, Gregory CA, Molnar P, Cui X, Jalota S, Bhaduri SB, Boland T (2006) Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials 27(19):3580–3588

    CAS  Google Scholar 

  226. Zhu K, Shin SR, van Kempen T, Li YC, Ponraj V, Nasajpour A, Lin YD (2017) Gold nanocomposite bioink for printing 3D cardiac constructs. Adv Funct Mater 27(12):1605352

    Google Scholar 

  227. Cui X, Breitenkamp K, Finn MG, Lotz M, D’Lima DD (2012) Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng Part A 18:1304–1312

    CAS  Google Scholar 

  228. Pirlo RK, Wu P, Liu J, Ringeisen B (2012) PLGA/hydrogel biopapers as a stackable substrate for printing HUVEC networks via BioLP™. Biotechnol Bioeng 109:262–273

    CAS  Google Scholar 

  229. Bandyopadhyay A, Dewangan VK, Vajanthri KY, Poddar S, Mahto SK (2018) Easy and affordable method for rapid prototyping of tissue models in vitro using three-dimensional bioprinting. Biocybern Biomed Eng 38:158–169

    Google Scholar 

  230. Snyder JE, Hamid Q, Wang C, Chang R, Emami K, Wu H, Sun W (2011) Bioprinting cell-laden matrigel for radioprotection study of liver by pro-drug conversion in a dual-tissue microfluidic chip. Biofabrication 3:034112

    CAS  Google Scholar 

  231. Isaacson A, Swioklo S, Connon CJ (2018) 3D bioprinting of a corneal stroma equivalent. Exp Eye Res 173:188–193

    CAS  Google Scholar 

  232. Agrawal G, Aung A, Varghese S (2017) Skeletal muscle-on-a-chip: an in vitro model to evaluate tissue formation and injury. Lab Chip 17:3447–3461

    CAS  Google Scholar 

  233. Massa S, Sakr MA, Seo J, Bandaru P, Arneri A, Bersini S, Zare-Eelanjegh E, Jalilian E, Cha B-H, Antona S et al (2017) Bioprinted 3D vascularized tissue model for drug toxicity analysis. Biomicrofluidics 11:044109

    Google Scholar 

  234. Datta S, Das A, Sasmal P, Bhutoria S, Roy Chowdhury A, Datta P (2018) Alginate-poly(amino acid) extrusion printed scaffolds for tissue engineering applications. Int J Polym Mater Polym Biomater. https://doi.org/10.1080/00914037.2018.1539988

    Article  Google Scholar 

  235. Tseng H, Gage JA, Shen T, Haisler WL, Neeley SK, Shiao S, Raphael RMA (2015) Spheroid toxicity assay using magnetic 3D bioprinting and real-time mobile device-based imaging. Sci Rep 5:13987

    CAS  Google Scholar 

Download references

Funding

Funding was provided by the Science and Engineering Research Board, Department of Science and Technology, Govt. of India (ECR/2015/000458) and the Department of Biotechnology, Govt. of India (BT/RLF/Re-entry/07/2015).

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, IIT Hyderabad, Kandi, Sangareddy, Telangana, 502285, India

    Shibu Chameettachal, Sriya Yeleswarapu, Shyama Sasikumar, Priyanshu Shukla, Purva Hibare, Ashis Kumar Bera, Sri Sai Ramya Bojedla & Falguni Pati

Authors
  1. Shibu Chameettachal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sriya Yeleswarapu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shyama Sasikumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Priyanshu Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Purva Hibare
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ashis Kumar Bera
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sri Sai Ramya Bojedla
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Falguni Pati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Falguni Pati.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chameettachal, S., Yeleswarapu, S., Sasikumar, S. et al. 3D Bioprinting: Recent Trends and Challenges. J Indian Inst Sci 99, 375–403 (2019). https://doi.org/10.1007/s41745-019-00113-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41745-019-00113-z

Search

Navigation