AccScience Publishing / IJB / Volume 10 / Issue 1 / DOI: 10.36922/ijb.1972
Cite this article
288
Download
970
Views
Journal Browser
Volume | Year
Issue
Search
News and Announcements
View All
REVIEW

Application of biomaterial-based three-dimensional bioprinting for organ-on-a-chip fabrication

Joeng Ju Kim1,2 Mihyeon Bae1,2 Jongmin Kim1,2 Dong-Woo Cho1,2*
Show Less
1 Department of Mechanical Engineering, Pohang University of Science and Technology (POSTECH), Pohang, Kyungbuk, Republic of Korea
2 POSTECH-Catholic Biomedical Engineering Institute, Pohang University of Science and Technology (POSTECH), Pohang, Kyungbuk, Republic of Korea
IJB 2024, 10(1), 1972 https://doi.org/10.36922/ijb.1972
Submitted: 6 October 2023 | Accepted: 6 November 2023 | Published: 2 January 2024
(This article belongs to the Special Issue 3D Bioprinting Hydrogels and Organ-On-Chip)
© 2024 by the 2024 Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

An organ-on-a-chip is a microfluidic device that simulates the microenvironment of organs, facilitating the study of human physiology and disease mechanisms. Through the integration of tissue engineering and micromachining technologies, it effectively manages the cellular microenvironment and implements tissue-specific functions and physiological responses with high fidelity. Several factors must be appropriately considered in the fabrication of an organ-on-a-chip, including the choice of biomaterials to simulate the extracellular matrix (ECM), selection of cells constituting the target organ, incorporation of humanized design to realize the primary function and structure of the organ, and the use of appropriate biofabrication methods to build a tissue-specific environment. Notably, three-dimensional (3D) bioprinting has emerged as a promising method for biofabricating organ-on-a-chip. Three-dimensional bioprinting offers versatility in adapting to various biomaterials with different physical properties, allowing precise control of 3D cell arrays and facilitating cyclic movements of fluidic flow within microfluidic platforms. These capabilities enable the precise fabrication of organ-on-a-chip that reflects tissue-specific functions and microenvironments. Additionally, 3D-bioprinted organ-on-a-chip can serve as a disease-on-a-chip platform, achieved through the implementation of pathophysiological environments and integration with devices such as bioreactors. Their significance in pharmacology research lies in their exceptional resemblance to the 3D microenvironment structure of actual organs, which are conducive for the validation of sequential mechanism of drug action. This review describes recent examples of organ-on-a-chip applications for various organs and state-of-the-art 3D bioprinting techniques employed in organ-on-a-chip fabrication. The discussion extends to the future prospects of this technology, encompassing aspects such as commercialization through mass production and its potential application in personalized medicine or drug-screening platforms. Serving as a relevant guide, this review offers insights for future research and developments in in vitro micromodel fabrication.

Keywords
3D bioprinting
Organ-on-a-chip
Disease-on-a-chip
Biomaterial
Bioink
Hydrogel
Funding
This work was supported by the National Research Foundation (NRF) of Korea grant, funded by the Korean Government (MSIP) (NRF-2022R1A2C3004300), and the Korean Fund for Regenerative Medicine funded by the Ministry of Science and ICT, and the Ministry of Health and Welfare, Republic of Korea (22A0106L1).
References
  1. Ingber DE. Human organs-on-chips for disease modelling, drug development and personalized medicine. Nat Rev Genet. 2022;23(8): 467-491. doi: 10.1038/s41576-022-00466-9
  2. Golding H, Khurana S, Zaitseva M. What is the predictive value of animal models for vaccine efficacy in humans? The importance of bridging studies and species-independent correlates of protection. Cold Spring Harb Perspect Biol. 2018;10(4): a028902. doi: 10.1101/cshperspect.a028902
  3. Seok J, Warren HS, Cuenca AG, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A. 2013;110(9): 3507-3512. doi: 10.1073/pnas.1222878110
  4. Franco R, Cedazo-Minguez A. Successful therapies for Alzheimer’s disease: why so many in animal models and none in humans? Front Pharmacol. 2014;5: 146. doi: 10.3389/fphar.2014.00146
  5. Kostewicz ES, Abrahamsson B, Brewster M, et al. In vitro models for the prediction of in vivo performance of oral dosage forms. Eur J Pharm Sci. 2014;57: 342-366. doi: 10.1016/j.ejps.2013.08.024
  6. Low LA, Mummery C, Berridge BR, Austin CP, Tagle DA. Organs-on-chips: into the next decade. Nat Rev Drug Discov. 2021;20(5): 345-361. doi: 10.1038/s41573-020-0079-3
  7. Zervantonakis IK, Kothapalli CR, Chung S, Sudo R, Kamm RD. Microfluidic devices for studying heterotypic cell-cell interactions and tissue specimen cultures under controlled microenvironments. Biomicrofluidics. 2011;5(1): 013406. doi: 10.1063/1.3553237
  8. Huh D, Hamilton GA, Ingber DE. From 3D cell culture to organs-on-chips. Trends Cell Biol. 2011;21(12): 745-754. doi: 10.1016/j.tcb.2011.09.005
  9. Shamir ER, Ewald AJ. Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat Rev Mol Cell Biol. 2014;15(10): 647-664. doi: 10.1038/nrm3873
  10. Fatehullah A, Tan SH, Barker N. Organoids as an in vitro model of human development and disease. Nat Cell Biol. 2016;18(3): 246-254. doi: 10.1038/ncb3312
  11. Chinta MS, desJardins-Park HE, Wan DC, Longaker MT. “Tissues in a dish”: a review of organoids in plastic surgery. Plast Reconstr Surg Glob Open. 2020;8(4): e2787. doi: 10.1097/GOX.0000000000002787
  12. Vazin T, Freed WJ. Human embryonic stem cells: derivation, culture, and differentiation: a review. Restor Neurol Neurosci. 2010;28(4): 589-603. doi: 10.3233/RNN-2010-0543
  13. Klicks J, von Molitor E, Ertongur-Fauth T, Rudolf R, Hafner M. In vitro skin three-dimensional models and their applications. J Cell Biotechnol. 2017;3(1): 21-39. doi: 10.3233/JCB-179004
  14. Leung CM, De Haan P, Ronaldson-Bouchard K, et al. A guide to the organ-on-a-chip. Nat Rev Methods Primers. 2022;2(1): 33. doi: 10.1038/s43586-022-00118-6
  15. Vanaei S, Parizi M, Salemizadehparizi F, Vanaei HR. An overview on materials and techniques in 3D bioprinting toward biomedical application. Eng Regen. 2021;2: 1-18. doi: 10.1016/j.engreg.2020.12.001
  16. Gungor-Ozkerim PS, Inci I, Zhang YS, Khademhosseini A, Dokmeci MR. Bioinks for 3D bioprinting: an overview. Biomater Sci. 2018;6(5): 915-946. doi: 10.1039/c7bm00765e
  17. Lee H, Cho D-W. One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3D bioprinting technology. Lab Chip. 2016;16(14): 2618-2625. doi: 10.1039/C6LC00450D
  18. Reid JA, Mollica PA, Johnson GD, Ogle RC, Bruno RD, Sachs PC. Accessible bioprinting: adaptation of a low-cost 3D-printer for precise cell placement and stem cell differentiation. Biofabrication. 2016;8(2): 025017. doi: 10.1088/1758-5090/8/2/025017
  19. Ozbolat IT, Moncal KK, Gudapati H. Evaluation of bioprinter technologies. Addit Manuf. 2017;13: 179-200. doi: 10.1016/j.addma.2016.10.003
  20. Carvalho V, Gonçalves I, Lage T, et al. 3D printing techniques and their applications to organ-on-a-chip platforms: a systematic review. Sensors. 2021;21(9): 3304. doi: 10.3390/s21093304
  21. Ambhorkar P, Rakin RH, Wang Z, Kumar H, Kim K. Biofabrication strategies for engineering heterogeneous artificial tissues. Addit Manuf. 2020;36: 101459. doi: 10.1016/j.addma.2020.101459
  22. Matai I, Kaur G, Seyedsalehi A, McClinton A, Laurencin CT. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials. 2020;226: 119536. doi: 10.1016/j.biomaterials.2019.119536
  23. Jung JW, Lee J-S, Cho D-W. Computer-aided multiple-head 3D printing system for printing of heterogeneous organ/ tissue constructs. Sci Rep. 2016;6(1): 21685. doi: 10.1038/srep21685
  24. Hockaday L, Kang K, Colangelo N, et al. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication. 2012;4(3): 035005. doi: 10.1088/1758-5082/4/3/035005
  25. Au AK, Lee W, Folch A. Mail-order microfluidics: evaluation of stereolithography for the production of microfluidic devices. Lab Chip. 2014;14(7): 1294-1301. doi: 10.1039/c3lc51360b
  26. Bhattacharjee N, Urrios A, Kang S, Folch A. The upcoming 3D-printing revolution in microfluidics. Lab Chip. 2016;16(10): 1720-1742. doi: 10.1039/c6lc00163g
  27. Lee H, Kim J, Choi Y, Cho D-W. Application of gelatin bioinks and cell-printing technology to enhance cell delivery capability for 3D liver fibrosis-on-a-chip development. ACS Biomater Sci Eng. 2020;6(4): 2469-2477. doi: 10.1021/acsbiomaterials.9b01735
  28. Skardal A, Atala A. Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng. 2015;43(3): 730-746. doi: 10.1007/s10439-014-1207-1
  29. Unagolla JM, Jayasuriya AC. Hydrogel-based 3D bioprinting: a comprehensive review on cell-laden hydrogels, bioink formulations, and future perspectives. Appl Mater Today. 2020;18: 100479. doi: 10.1016/j.apmt.2019.100479
  30. Murphy SV, Skardal A, Atala A. Evaluation of hydrogels for bio‐printing applications. J Biomed Mater Res Part A. 2013;101(1): 272-284. doi: 10.1002/jbm.a.34326
  31. Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem Rev. 2001;101(7): 1869-1880. doi: 10.1021/cr000108x
  32. Khademhosseini A, Langer R. Microengineered hydrogels for tissue engineering. Biomaterials. 2007;28(34): 5087-5092. doi: 10.1016/j.biomaterials.2007.07.021
  33. Jang J, Yi H-G, Cho D-W. 3D printed tissue models: present and future. ACS Biomater Sci Eng. 2016;2(10): 1722-1731. doi: 10.1021/acsbiomaterials.6b00129
  34. Peng W, Unutmaz D, Ozbolat IT. Bioprinting towards physiologically relevant tissue models for pharmaceutics. Trends Biotechnol. 2016;34(9): 722-732. doi: 10.1016/j.tibtech.2016.05.013
  35. Malda J, Visser J, Melchels FP, et al. 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater. 2013;25(36): 5011-5028. doi: 10.1002/adma.201302042
  36. Cen L, Liu W, Cui L, Zhang W, Cao Y. Collagen tissue engineering: development of novel biomaterials and applications. Pediatr Res. 2008;63(5): 492-496. doi: 10.1203/PDR.0b013e31816c5bc3
  37. Parenteau-Bareil R, Gauvin R, Berthod F. Collagen-based biomaterials for tissue engineering applications. Materials. 2010;3(3): 1863-1887. doi: 10.3390/ma3031863
  38. Persaud A, Maus A, Strait L, Zhu D. 3D bioprinting with live cells. Eng Regen. 2022;3(3): 292-309. doi: 10.1016/j.engreg.2022.07.002
  39. Gaudet ID, Shreiber DI. Characterization of methacrylated type-I collagen as a dynamic, photoactive hydrogel. Biointerphases. 2012;7(1): 25. doi: 10.1007/s13758-012-0025-y
  40. Shi H, Li Y, Xu K, Yin J. Advantages of photo-curable collagen-based cell-laden bioinks compared to methacrylated gelatin (GelMA) in digital light processing (DLP) and extrusion bioprinting. Mater Today Bio. 2023;23: 100799. doi: 10.1016/j.mtbio.2023.100799
  41. Khoeini R, Nosrati H, Akbarzadeh A, et al. Natural and synthetic bioinks for 3D bioprinting. Adv NanoBiomed Res. 2021;1(8): 2000097. doi: 10.1002/anbr.202000097
  42. Shin JH, Kang H-W. The development of gelatin-based bio-ink for use in 3D hybrid bioprinting. Int J Prec Eng Manuf. 2018;19: 767-771. doi: 10.1007/s12541-018-0092-1
  43. Chimene D, Kaunas R, Gaharwar AK. Hydrogel bioink reinforcement for additive manufacturing: a focused review of emerging strategies. Adv Mater. 2020;32(1): 1902026. doi: 10.1002/adma.201902026
  44. Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials. 2010;31(21): 5536-5544. doi: 10.1016/j.biomaterials.2010.03.064
  45. Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37(1): 106-126. doi: 10.1016/j.progpolymsci.2011.06.003
  46. Axpe E, Oyen ML. Applications of alginate-based bioinks in 3D bioprinting. Int J Mol Sci. 2016;17(12): 1976. doi: 10.3390/ijms17121976
  47. Jia J, Richards DJ, Pollard S, et al. Engineering alginate as bioink for bioprinting. Acta Biomater. 2014;10(10): 4323-4331. doi: 10.1016/j.actbio.2014.06.034
  48. Yang X, Lu Z, Wu H, Li W, Zheng L, Zhao J. Collagen-alginate as bioink for three-dimensional (3D) cell printing based cartilage tissue engineering. Mater Sci Eng C. 2018;83: 195-201. doi: 10.1016/j.msec.2017.09.002
  49. Othman SA, Soon CF, Ma NL, et al. Alginate-gelatin bioink for bioprinting of hela spheroids in alginate-gelatin hexagon shaped scaffolds. Polym Bull. 2021;78: 6115-6135. doi: 10.1007/s00289-020-03421-y
  50. Compaan AM, Christensen K, Huang Y. Inkjet bioprinting of 3D silk fibroin cellular constructs using sacrificial alginate. ACS Biomater Sci Eng. 2017;3(8): 1519-1526. doi: 10.1021/acsbiomaterials.6b00432
  51. Gao Q, Kim B-S, Gao G. Advanced strategies for 3D bioprinting of tissue and organ analogs using alginate hydrogel bioinks. Mar Drugs. 2021;19(12): 708. doi: 10.3390/md19120708
  52. Choi Y-J, Cho D-W, Lee H. Development of silk fibroin scaffolds by using indirect 3D-bioprinting technology. Micromachines. 2022;13(1): 43. doi: 10.3390/mi13010043
  53. Zheng Z, Wu J, Liu M, et al. 3D bioprinting of self‐standing silk‐based bioink. Adv Healthc Mater. 2018;7(6): 1701026. doi: 10.1002/adhm.201701026
  54. Rodriguez MJ, Brown J, Giordano J, Lin SJ, Omenetto FG, Kaplan DL. Silk based bioinks for soft tissue reconstruction using 3-dimensional (3D) printing with in vitro and in vivo assessments. Biomaterials. 2017;117: 105-115. doi: 10.1016/j.biomaterials.2016.11.046
  55. Pati F, Jang J, Ha D-H, et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun. 2014;5(1): 3935. doi: 10.1038/ncomms4935
  56. Kim BS, Das S, Jang J, Cho D-W. Decellularized extracellular matrix-based bioinks for engineering tissue-and organ-specific microenvironments. Chem Rev. 2020;120(19): 10608-10661. doi: 10.1021/acs.chemrev.9b00808
  57. Choudhury D, Tun HW, Wang T, Naing MW. Organ-derived decellularized extracellular matrix: a game changer for bioink manufacturing? Trends Biotechnol. 2018;36(8):787-805. doi: 10.1016/j.tibtech.2018.03.003
  58. Choudhury D, Yee M, Sheng ZLJ, Amirul A, Naing MW. Decellularization systems and devices: state-of-the-art. Acta Biomater. 2020;115: 51-59. doi: 10.1016/j.actbio.2020.07.060
  59. Kim H, Kang B, Cui X, et al. Light‐activated decellularized extracellular matrix‐based bioinks for volumetric tissue analogs at the centimeter scale. Adv Funct Mater. 2021;31(32): 2011252. doi: 10.1002/adfm.202011252
  60. Asti A, Gioglio L. Natural and synthetic biodegradable polymers: different scaffolds for cell expansion and tissue formation. Int J Artif Organs. 2014;37(3): 187-205. doi: 10.530/ijao.5000307
  61. Griffin M, Castro N, Bas O, Saifzadeh S, Butler P, Hutmacher DW. The current versatility of polyurethane three-dimensional printing for biomedical applications. Tissue Eng Part B Rev. 2020;26(3): 272-283. doi: 10.1089/ten.TEB.2019.0224
  62. Woodruff MA, Hutmacher DW. The return of a forgotten polymer—polycaprolactone in the 21st century. Prog Polym Sci. 2010;35(10): 1217-1256. doi: 10.1016/j.progpolymsci.2010.04.002
  63. Kim BS, Jang J, Chae S, et al. Three-dimensional bioprinting of cell-laden constructs with polycaprolactone protective layers for using various thermoplastic polymers. Biofabrication. 2016;8(3): 035013. doi: 10.1088/1758-5090/8/3/035013
  64. Wu W, DeConinck A, Lewis JA. Omnidirectional printing of 3D microvascular networks. Adv Mater. 2011;23(24): H178-H183. doi: 10.1002/adma.201004625
  65. Homan KA, Kolesky DB, Skylar-Scott MA, et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep. 2016;6(1): 34845. doi: 10.1038/srep34845
  66. Campbell SB, Wu Q, Yazbeck J, Liu C, Okhovatian S, Radisic M. Beyond polydimethylsiloxane: alternative materials for fabrication of organ-on-a-chip devices and microphysiological systems. ACS Biomater Sci Eng. 2020;7(7): 2880-2899. doi: 10.1021/acsbiomaterials.0c00640
  67. Duffy DC, McDonald JC, Schueller OJ, Whitesides GM. Rapid prototyping of microfluidic systems in poly (dimethylsiloxane). Anal Chem. 1998;70(23): 4974-4984. doi: 10.1021/ac980656z
  68. Miranda I, Souza A, Sousa P, et al. Properties and applications of PDMS for biomedical engineering: a review. J Funct Biomater. 2021;13(1): 2. doi: 10.3390/jfb13010002
  69. Carneiro J, Lima R, Campos J, Miranda JM. A microparticle blood analogue suspension matching blood rheology. Soft Matter. 2021;17(14): 3963-3974. doi: 10.1039/D1SM00106J
  70. Wu X, Kim S-H, Ji C-H, Allen MG. A solid hydraulically amplified piezoelectric microvalve. J Micromech Microeng. 2011;21(9): 095003. doi: 10.1088/0960-1317/21/9/095003
  71. Rao H-X, Liu F-N, Zhang Z-Y. Preparation and oxygen/ nitrogen permeability of PDMS crosslinked membrane and PDMS/tetraethoxysilicone hybrid membrane. J Membr Sci. 2007;303(1-2): 132-139. doi: 10.1016/j.memsci.2007.07.002
  72. Shrestha J, Ghadiri M, Shanmugavel M, et al. A rapidly prototyped lung-on-a-chip model using 3D-printed molds. Organs Chip. 2019;1: 100001. doi: 10.1016/j.ooc.2020.100001
  73. Jung JP, Bhuiyan DB, Ogle BM. Solid organ fabrication: comparison of decellularization to 3D bioprinting. Biomater Res. 2016;20: 1-11. doi: 10.1186/s40824-016-0074-2
  74. Mandrycky C, Wang Z, Kim K, Kim D-H. 3D bioprinting for engineering complex tissues. Biotechnol Adv. 2016;34(4): 422-434. doi: 10.1016/j.biotechadv.2015.12.011
  75. Lee J-S, Hong JM, Jung JW, Shim J-H, Oh J-H, Cho D-W. 3D printing of composite tissue with complex shape applied to ear regeneration. Biofabrication. 2014;6(2): 024103. doi: 10.1088/1758-5082/6/2/024103
  76. Lee JW, Choi Y-J, Yong W-J, et al. Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication. 2016;8(1): 015007. doi: 10.1088/1758-5090/8/1/015007
  77. Lee H, Yoo JJ, Kang H-W, Cho D-W. Investigation of thermal degradation with extrusion-based dispensing modules for 3D bioprinting technology. Biofabrication. 2016;8(1): 015011. doi: 10.1088/1758-5090/8/1/015011
  78. Tan Y, Richards DJ, Trusk TC, et al. 3D printing facilitated scaffold-free tissue unit fabrication. Biofabrication. 2014;6(2): 024111. doi: 10.1088/1758-5082/6/2/024111
  79. Cheng E, Yu H, Ahmadi A, Cheung KC. Investigation of the hydrodynamic response of cells in drop on demand piezoelectric inkjet nozzles. Biofabrication. 2016;8(1):015008. doi: 10.1088/1758-5090/8/1/015008
  80. Cui X, Dean D, Ruggeri ZM, Boland T. Cell damage evaluation of thermal inkjet printed Chinese hamster ovary cells. Biotechnol Bioeng. 2010;106(6): 963-969. doi: 10.1002/bit.22762
  81. Xu T, Gregory CA, Molnar P, et al. Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials. 2006;27(19): 3580-3588. doi: 10.1016/j.biomaterials.2006.01.048
  82. Saunders RE, Gough JE, Derby B. Delivery of human fibroblast cells by piezoelectric drop-on-demand inkjet printing. Biomaterials. 2008;29(2): 193-203. doi: 10.1016/j.biomaterials.2007.09.032
  83. Tasoglu S, Demirci U. Bioprinting for stem cell research. Trends Biotechnol. 2013;31(1): 10-19. doi: 10.1016/j.tibtech.2012.10.005
  84. Singh M, Haverinen HM, Dhagat P, Jabbour GE. Inkjet printing—process and its applications. Adv Mater. 22(6): 673-685. doi: 10.1002/adma.200901141
  85. Koch L, Deiwick A, Schlie S, et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng. 2012;109(7):1855-1863. doi: 10.1002/bit.24455
  86. Yan J, Huang Y, Chrisey DB. Laser-assisted printing of alginate long tubes and annular constructs. Biofabrication. 2012;5(1): 015002. doi: 10.1088/1758-5082/5/1/015002
  87. Pages E, Rémy M, Keriquel V, Correa MM, Guillotin B, Guillemot F. Creation of highly defined mesenchymal stem cell patterns in three dimensions by laser-assisted bioprinting. J Nanotechnol Eng Med. 2015;6(2): 021006. doi: 10.1115/1.4031217
  88. Park JH, Jang J, Lee J-S, Cho D-W. Three-dimensional printing of tissue/organ analogues containing living cells. Ann Biomed Eng. 2017;45: 180-194. doi: 10.1007/s10439-016-1611-9
  89. Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR. Organ printing: tissue spheroids as building blocks. Biomaterials. 2009;30(12): 2164-2174. doi: 10.1016/j.biomaterials.2008.12.084
  90. Kim BS, Ahn M, Cho W-W, Gao G, Jang J, Cho D-W. Engineering of diseased human skin equivalent using 3D cell printing for representing pathophysiological hallmarks of type 2 diabetes in vitro. Biomaterials. 2021;272: 120776. doi: 10.1016/j.biomaterials.2021.120776
  91. Anada T, Pan C-C, Stahl AM, et al. Vascularized bone-mimetic hydrogel constructs by 3D bioprinting to promote osteogenesis and angiogenesis. Int J Mol Sci. 2019;20(5): 1096. doi: 10.3390/ijms20051096
  92. Gao G, Park W, Kim BS, et al. Construction of a novel in vitro atherosclerotic model from geometry‐tunable artery equivalents engineered via in‐bath coaxial cell printing. Adv Funct Mater. 2021;31(10): 2008878. doi: 10.1002/adfm.202008878
  93. Lin NY, Homan KA, Robinson SS, et al. Renal reabsorption in 3D vascularized proximal tubule models. Proc Natl Acad Sci U S A. 2019;116(12): 5399-5404. doi: 10.1073/pnas.1815208116
  94. Singh NK, Han W, Nam SA, et al. Three-dimensional cell-printing of advanced renal tubular tissue analogue. Biomaterials. 2020;232: 119734. doi: 10.1016/j.biomaterials.2019.119734
  95. Menon GK. New insights into skin structure: scratching the surface. Adv Drug Deliv Rev. 2002;54: S3-S17. doi: 10.1016/s0169-409x(02)00121-7
  96. Van Gele M, Geusens B, Brochez L, Speeckaert R, Lambert J. Three-dimensional skin models as tools for transdermal drug delivery: challenges and limitations. Expert Opin Drug Deliv. 2011;8(6): 705-720. doi: 10.1517/17425247.2011.568937
  97. Lumpkin EA, Caterina MJ. Mechanisms of sensory transduction in the skin. Nature. 2007;445(7130): 858-865. doi: 10.1038/nature05662
  98. Huang S, Xu Y, Wu C, Sha D, Fu X. In vitro constitution and in vivo implantation of engineered skin constructs with sweat glands. Biomaterials. 2010;31(21): 5520-5525. doi: 10.1016/j.biomaterials.2010.03.060
  99. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T. Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science. 1981;211(4486): 1052-1054. doi: 10.1126/science.7008197
  100. Groeber F, Holeiter M, Hampel M, Hinderer S, Schenke- Layland K. Skin tissue engineering—in vivo and in vitro applications. Adv Drug Deliv Rev. 2011;63(4-5): 352-366. doi: 10.1016/j.addr.2011.01.005
  101. Clement AL, Moutinho Jr TJ, Pins GD. Micropatterned dermal–epidermal regeneration matrices create functional niches that enhance epidermal morphogenesis. Acta Biomater. 2013;9(12): 9474-9484. doi: 10.1016/j.actbio.2013.08.017
  102. Lammers G, Roth G, Heck M, et al. Construction of a microstructured collagen membrane mimicking the papillary dermis architecture and guiding keratinocyte morphology and gene expression. Macromol Biosci. 2012;12(5): 675-691. doi: 10.1002/mabi.201100443
  103. Hudon V, Berthod F, Black A, Damour O, Germain L, Auger FA. A tissue‐engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary‐like tube formation in vitro. Br J Dermatol. 2003;148(6): 1094-1104. doi: 10.1046/j.1365-2133.2003.05298.x
  104. Kim BS, Gao G, Kim JY, Cho D-W. 3D cell printing of perfusable vascularized human skin equivalent composed of epidermis, dermis, and hypodermis for better structural recapitulation of native skin. Adv Healthc Mater. 2019;8(7): 1801019. doi: 10.1002/adhm.201801019
  105. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest. 2007;117(5): 1219-1222. doi: 10.1172/JCI32169
  106. Ramasamy S, Davoodi P, Vijayavenkataraman S, et al. Optimized construction of a full thickness human skin equivalent using 3D bioprinting and a PCL/collagen dermal scaffold. Bioprinting. 2021;21: e00123. doi: 10.1016/j.bprint.2020.e00123
  107. Ng WL, Qi JTZ, Yeong WY, Naing MW. Proof-of-concept: 3D bioprinting of pigmented human skin constructs. Biofabrication. 2018;10(2): 025005. doi: 10.1088/1758-5090/aa9e1e
  108. Saunders J, Elbestawi M, Fang Q. Ultrafast laser additive manufacturing: a review. J Manuf Mater Process. 2023; 7(3): 89. doi: 10.3390/jmmp7030089
  109. Niehues H, Bouwstra JA, El Ghalbzouri A, Brandner JM, Zeeuwen PLJM, van den Bogaard EH. 3D skin models for 3R research: the potential of 3D reconstructed skin models to study skin barrier function. Exp Dermatol. 2018;27(5): 501-511. doi: 10.1111/exd.13531
  110. Sun W, Liu Z, Xu J, et al. 3D skin models along with skin-on-a-chip systems: a critical review. Chin Chem Lett. 2023; 34(5): 107819. doi: 10.1016/j.cclet.2022.107819
  111. Folkman J, D’Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87(7): 1153-1155. doi: 10.1016/s0092-8674(00)81810-3
  112. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature. 2005;436(7048): 193-200. doi: 10.1038/nature03875
  113. L’heureux N, Pâquet S, Labbé R, Germain L, Auger FA. A completely biological tissue‐engineered human blood vessel. FASEB J. 1998;12(1): 47-56. doi: 10.1096/fasebj.12.1.47
  114. Jones EA, le Noble F, Eichmann A. What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology. 2006;21(6): 388-395. doi: 10.1152/physiol.00020.2006
  115. Dornhof J, Kieninger J, Muralidharan H, Maurer J, Urban GA, Weltin A. Microfluidic organ-on-chip system for multi-analyte monitoring of metabolites in 3D cell cultures. Lab Chip. 2022;22(2): 225-239. doi: 10.1039/D1LC00689D
  116. Skardal A, Zhang J, McCoard L, Xu X, Oottamasathien S, Prestwich GD. Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Eng Part A. 2010;16(8): 2675-2685. doi: 10.1089/ten.TEA.2009.0798
  117. Gao G, Lee JH, Jang J, et al. 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. 2017;27(33): 1700798. doi: 10.1002/adfm.201700798
  118. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352(16): 1685-1695. doi: 10.1056/NEJMra043430
  119. Cui H, Zhu W, Huang Y, et al. In vitro and in vivo evaluation of 3D bioprinted small-diameter vasculature with smooth muscle and endothelium. Biofabrication. 2019;12(1): 015004. doi: 10.1088/1758-5090/ab402c
  120. Zhang Y, Kumar P, Lv S, et al. Recent advances in 3D bioprinting of vascularized tissues. Mater Des. 2021;199: 109398. doi: 10.1016/j.matdes.2020.109398
  121. Murugesan K, Anandapandian PA, Sharma SK, Kumar MV. Comparative evaluation of dimension and surface detail accuracy of models produced by three different rapid prototype techniques. J Indian Prosthodont Soc. 2012;12:16-20. doi: 10.1007/s13191-011-0103-8
  122. Mota C, Camarero-Espinosa S, Baker MB, Wieringa P, Moroni L. Bioprinting: from tissue and organ development to in vitro models. Chem Rev. 2020;120(19): 10547-10607. doi: 10.1021/acs.chemrev.9b00789
  123. Reint G, Rak-Raszewska A, Vainio SJ. Kidney development and perspectives for organ engineering. Cell Tissue Res. 2017;369: 171-183. doi: 10.1007/s00441-017-2616-x
  124. Finco DR. Kidney Function. London, United Kingdom: Elsevier; 1997. doi: 10.1016/B978-012396305-5/50018-X
  125. Singh NK, Kim JY, Lee JY, et al. Coaxial cell printing of a human glomerular model: an in vitro glomerular filtration barrier and its pathophysiology. Biofabrication. 2023;15(2): 024101. doi: 10.1088/1758-5090/acad2c
  126. King SM, Higgins JW, Nino CR, et al. 3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing. Front Physiol. 2017;8: 123. doi: 10.3389/fphys.2017.00123
  127. Homan KA, Gupta N, Kroll KT, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods. 2019;16(3): 255-262. doi: 10.1038/s41592-019-0325-y
  128. Lawlor KT, Vanslambrouck JM, Higgins JW, et al. Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation. Nat Mater. 2021;20(2): 260-271. doi: 10.1038/s41563-020-00853-9
  129. Wang D, Gust M, Ferrell N. Kidney-on-a-chip: mechanical stimulation and sensor integration. Sensors. 2022; 22(18): 6889. doi: 10.3390/s22186889
  130. Kim S, Takayama S. Organ-on-a-chip and the kidney. Kidney Res Clin Pract. 2015;34(3): 165-169.

doi: 10.1016/j.krcp.2015.08.001

  1. Cheung KL, Lafayette RA. Renal physiology of pregnancy. Adv Chronic Kidney Dis. 2013;20(3): 209-214. doi: 10.1053/j.ackd.2013.01.012
  2. Fransen MF, Addario G, Bouten CV, Halary F, Moroni L, Mota C. Bioprinting of kidney in vitro models: cells, biomaterials, and manufacturing techniques. Essays Biochem. 2021;65(3): 587-602. doi: 10.1042/EBC20200158
  3. Lasli S, Kim H J, Lee K, et al. A human liver‐on‐a‐chip platform for modeling nonalcoholic fatty liver disease. Adv Biosyst. 2019;3(8): 1900104. doi: 10.1002/adbi.201900104
  4. Tajiri K, Shimizu Y. Liver physiology and liver diseases in the elderly. World J Gastroenterol. 2013;19(46): 8459. doi: 10.3748/wjg.v19.i46.8459
  5. Bellentani S. The epidemiology of non‐alcoholic fatty liver disease. Liver Int. 2017;37: 81-84. doi: 10.1111/liv.13299
  6. Huang D, Gibeley SB, Xu C, et al. Engineering liver microtissues for disease modeling and regenerative medicine. Adv Funct Mater. 2020;30(44): 1909553. doi: 10.1002/adfm.201909553
  7. Du Y, Li N, Yang H, et al. Mimicking liver sinusoidal structures and functions using a 3D-configured microfluidic chip. Lab Chip. 2017;17(5): 782-794. doi: 10.1039/C6LC01374K
  8. Wisse E, De Zanger R, Charels K, Van Der Smissen P, McCuskey RS. The liver sieve: considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology. 1985;5(4): 683-692. doi: 10.1002/hep.1840050427
  9. Berger DR, Ware BR, Davidson MD, Allsup SR, Khetani SR. Enhancing the functional maturity of induced pluripotent stem cell–derived human hepatocytes by controlled presentation of cell–cell interactions in vitro. Hepatology. 2015;61(4): 1370-1381. doi: 10.1002/hep.27621
  10. Rennert K, Steinborn S, Gröger M, et al. A microfluidically perfused three dimensional human liver model. Biomaterials. 2015;71: 119-131. doi: 10.1016/j.biomaterials.2015.08.043
  11. Taymour R, Kilian D, Ahlfeld T, Gelinsky M, Lode A. 3D bioprinting of hepatocytes: core–shell structured co- cultures with fibroblasts for enhanced functionality. Sci Rep. 2021;11(1): 5130. doi: 10.1038/s41598-021-84384-6
  12. Kang HK, Sarsenova M, Kim D-H, et al. Establishing a 3D in vitro hepatic model mimicking physiologically relevant to in vivo state. Cells. 2021;10(5): 1268. doi: 10.3390/cells10051268
  13. Wang T, Du Z, Zhu F, et al. Comorbidities and multi-organ injuries in the treatment of COVID-19. Lancet. 2020;395(10228): e52. doi: 10.1016/S0140-6736(20)30558-4
  14. Deng J, Wei W, Chen Z, et al. Engineered liver-on-a-chip platform to mimic liver functions and its biomedical applications: a review. Micromachines. 2019;10(10): 676. doi: 10.3390/mi10100676
  15. Jin B, Liu Y, Du S, et al. Current trends and research topics regarding liver 3D bioprinting: a bibliometric analysis research. Front Cell Dev Biol. 2022;10: 1047524. doi: 10.3389/fcell.2022.1047524
  16. Sahlman P, Nissinen M, Puukka P, et al. Genetic and lifestyle risk factors for advanced liver disease among men and women. J Gastroenterol Hepatol. 2020;35(2): 291-298. doi: 10.1111/jgh.14770
  17. Yi H-G, Lee H, Cho D-W. 3D printing of organs-on-chips. Bioengineering. 2017;4(1): 10. doi: 10.3390/bioengineering4010010
  18. Miri AK, Mirzaee I, Hassan S, et al. Effective bioprinting resolution in tissue model fabrication. Lab Chip. 2019;19(11): 2019-2037. doi: 10.1039/C8LC01037D
  19. Brodal P. The Central Nervous System: Structure and Function. New York, United States: Oxford University Press; 2004. doi: 10.1007/s00415-004-0459-3
  20. LináKong Y. 3D printed nervous system on a chip. Lab Chip. 2016;16(8): 1393-1400. doi: 10.1039/C5LC01270H
  21. Zhang WJ, Liu W, Cui L, Cao Y. Tissue engineering of blood vessel. J Cell Mol Med. 2007;11(5): 945-957. doi: 10.1111/j.1582-4934.2007.00099.x
  22. Abramson DI. Blood Vessels and Lymphatics. London, United Kingdom: Elsevier; 2013.
  23. Nabel EG. Cardiovascular disease. N Engl J Med. 2003;349(1): 60-72. doi: 10.1056/NEJMra035098
  24. Zhang YS, Arneri A, Bersini S, et al. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials. 2016;110: 45-59. doi: 10.1016/j.biomaterials.2016.09.003
  25. Sharp AN, Heazell AE, Crocker IP, Mor G. Placental apoptosis in health and disease. Am J Reprod Immunol. 2010;64(3): 159-169. doi: 10.1111/j.1600-0897.2010.00837.x
  26. Kuo CY, Shevchuk M, Opfermann J, et al. Trophoblast– endothelium signaling involves angiogenesis and apoptosis in a dynamic bioprinted placenta model. Biotechnol Bioeng. 2019;116(1): 181-192. doi: 10.1002/bit.26850
  27. Kuo C-Y, Eranki A, Placone JK, et al. Development of a 3D printed, bioengineered placenta model to evaluate the role of trophoblast migration in preeclampsia. ACS Biomater Sci Eng. 2016;2(10): 1817-1826. doi: 10.1021/acsbiomaterials.6b00031
  28. Kim W, Kim G. Intestinal villi model with blood capillaries fabricated using collagen-based bioink and dual-cell-printing process. ACS Appl Mater Interfaces. 2018;10(48): 41185-41196. doi: 10.1021/acsami.8b17410
  29. Park JY, Ryu H, Lee B, et al. Development of a functional airway-on-a-chip by 3D cell printing. Biofabrication. 2018;11(1): 015002. doi: 10.1088/1758-5090/aae545
  30. Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science. 2010;328(5986): 1662-1668. doi: 10.1126/science.1188302
  31. O’Bryan CS, Bhattacharjee T, Niemi SR, et al. Three-dimensional printing with sacrificial materials for soft matter manufacturing. Mrs Bull. 2017;42(8): 571-577. doi: 10.1557/mrs.2017.167
  32. Jalili-Firoozinezhad S, Miranda CC, Cabral JM. Modeling the human body on microfluidic chips. Trends Biotechnol. 2021;39(8): 838-852. doi: 10.1016/j.tibtech.2021.01.004
  33. Sosa-Hernández JE, Villalba-Rodríguez AM, Romero- Castillo KD, et al. Organs-on-a-chip module: a review from the development and applications perspective. Micromachines. 2018;9(10): 536. doi: 10.3390/mi9100536
  34. Choi Y-J, Park H, Ha D-H, Yun H-S, Yi H-G, Lee H. 3D bioprinting of in vitro models using hydrogel-based bioinks. Polymers. 2021;13(3): 366. doi: 10.3390/polym13030366
  35. Yi H-G, Kim H, Kwon J, Choi Y-J, Jang J, Cho D-W. Application of 3D bioprinting in the prevention and the therapy for human diseases. Signal Transduct Target Ther. 2021;6(1): 177. doi: 10.1038/s41392-021-00566-8
  36. Chang R, Nam J, Sun W. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication–based direct cell writing. Tissue Eng Part A. 2008;14(1): 41-48. doi: 10.1089/ten.a.2007.0004
  37. Derby B. Printing and prototyping of tissues and scaffolds. Science. 2012;338(6109): 921-926. doi: 10.1126/science.1226340
  38. Amorim P, d’Ávila M, Anand R, Moldenaers P, Van Puyvelde P, Bloemen V. Insights on shear rheology of inks for extrusion-based 3D bioprinting. Bioprinting. 2021;22: e00129. doi: 10.1016/j.bprint.2021.e00129
  39. Ning L, Betancourt N, Schreyer DJ, Chen X. Characterization of cell damage and proliferative ability during and after bioprinting. ACS Biomater Sci Eng. 2018;4(11): 3906-3918. doi: 10.1021/acsbiomaterials.8b00714
  40. Li J, He L, Zhou C, et al. 3D printing for regenerative medicine: from bench to bedside. Mrs Bull. 2015;40(2): 145-154. doi: 10.1557/mrs.2015.5
  41. Bajaj P, Schweller RM, Khademhosseini A, West JL, Bashir R. 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu Rev Biomed Eng. 2014;16: 247-276. doi: 10.1146/annurev-bioeng-071813-105155
  42. Brassard J A, Nikolaev M, Hübscher T, Hofer M, Lutolf MP. Recapitulating macro-scale tissue self-organization through organoid bioprinting. Nat Mater. 2021;20(1): 22-29. doi: 10.1038/s41563-020-00803-5
  43. Gao B, Yang Q, Zhao X, Jin G, Ma Y, Xu F. 4D bioprinting for biomedical applications. Trends Biotechnol. 2016;34(9): 746-756. doi: 10.1016/j.tibtech.2016.03.004
  44. Kirillova A, Maxson R, Stoychev G, Gomillion CT, Ionov L. 4D biofabrication using shape‐morphing hydrogels. Adv Mater. 2017;29(46): 1703443. doi: 10.1002/adma.201703443
  45. Lee VK, Dai G. Three-dimensional bioprinting and tissue fabrication: prospects for drug discovery and regenerative medicine. Adv Healthc Technol. 2015;1: 23. doi: 10.2147/AHCT.S69191
  46. Hölzl K, Lin S, Tytgat L, Van Vlierberghe S, Gu L, Ovsianikov A. Bioink properties before, during and after 3D bioprinting. Biofabrication. 2016;8(3): 032002. doi: 10.1088/1758-5090/8/3/032002
  47. Chen EP, Toksoy Z, Davis BA, Geibel JP. 3D bioprinting of vascularized tissues for in vitro and in vivo applications. Front Bioeng Biotechnol. 2021;9: 664188. doi: 10.3389/fbioe.2021.664188
  48. Ke D, Niu C, Yang X. Evolution of 3D bioprinting-from the perspectives of bioprinting companies. Bioprinting. 2022;25: e00193. doi: 10.1016/j.bprint.2022.e00193
  49. Lee J, Kim KE, Bang S, Noh I, Lee C. A desktop multi-material 3D bio-printing system with open-source hardware and software. Int J Prec Eng Manuf. 2017;18: 605-612. doi: 10.1007/s12541-017-0072-x
  50. Fateri M, Gebhardt A. Introduction to additive manufacturing. In: Heinrich A, ed. 3D Printing of Optical Components. Cham: Springer; 2021: 1-22. doi: 10.1007/978-3-030-58960-8_1
  51. Wu Q, Liu J, Wang X, et al. Organ-on-a-chip: recent breakthroughs and future prospects. Biomed Eng Online. 2020;19: 1-19. doi: 10.1186/s12938-020-0752-0
  52. Kim JJ, Park JY, Nguyen VVT, et al. Pathophysiological reconstruction of a tissue‐specific multiple‐organ on‐a‐chip for type 2 diabetes emulation using 3D cell printing. Adv Funct Mater. 2023;33(22): 2213649. doi: 10.1002/adfm.202213649
  53. Craighead H. Future lab-on-a-chip technologies for interrogating individual molecules. Nature. 2006;442(7101):387-393. doi: 10.1038/nature05061
  54. Sakai S, Yoshii A, Sakurai S, Horii K, Nagasuna O. Silk fibroin nanofibers: a promising ink additive for extrusion three-dimensional bioprinting. Mater Today Bio. 2020;8: 100078. doi: 10.1016/j.mtbio.2020.100078
  55. Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials. Chem Rev. 2020;120(19): 10793-10833. doi: 10.1021/acs.chemrev.0c00008
  56. Yang H, Yang K-H, Narayan RJ, Ma S. Laser-based bioprinting for multilayer cell patterning in tissue engineering and cancer research. Essays Biochem. 2021;65(3): 409-416. doi: 10.1042/EBC20200093
Conflict of interest
The authors declare no conflicts of interest.
Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing