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The application of 3D bioprinting technology in liver manufacturing: Progress, challenges, and prospects

 

Yifan Hou1,2,3 ,  Xin Liu1,2* ,  Xinhuan Wang1,2 ,  Shen Ji1,2 ,  Qi Gu1,2,3*
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1 Key laboratory of Organ Regeneration and Reconstruction, State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, P. R. China
2 Beijing Institute for Stem Cell and Regenerative Medicine, Beijing, P. R. China
3 University of Chinese Academy of Sciences, Beijing, P. R. China
IJB, 3819 https://doi.org/10.36922/ijb.3819
Submitted: 1 June 2024 | Accepted: 12 July 2024 | Published: 29 August 2024
© 2024 by the 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/ )
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Abstract

Recreating the complexity of liver structure and the diversity of cells and functions in vitro remains a significant focus in liver tissue engineering. 3D bioprinting technology features advantages in personalized manufacturing, replicating complex internal structures, and precise arrangement of multi-materials and cells, thus holding vast potential in tissue engineering, particularly for liver manufacturing. In this review, we discuss the complexity of the liver structure and function, including its composition and both development and regeneration processes. We then analyze the current limitations in liver transplantation, e.g., donor organ shortage, and the shortcomings of various liver transplantation alternatives, highlighting the importance of 3D bioprinting for liver fabrication. Furthermore, the composition and properties of the bioinks used in the liver 3D-printing process and the corresponding research outcomes are discussed. Notably, we summarize the latest advances and challenges in the field of liver fabrication and explore future development directions, namely vascular and bile duct structures. In summation, this review can provide guidance and inspiration for future research and applications related to liver reconstruction and manufacturing.

Keywords
Liver fabrication
Bioprinting
Bioink
Vascularization
Funding
This research was supported by the National Natural Science Foundation of China (62127811, U23A20453, U21A20396, T2222029), the National Key Research and Development Program of China (2022YFA1104701), Initiative Scientific Research Program of Institute of Zoology (2023IOZ0101), and the CAS Engineering Laboratory for Intelligent Organ Manufacturing (KFJ-PTXM-039).
Conflict of interest
The authors declare no conflicts of interest.
References
  1. Lemaigre FP. Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology. 2009;137(1):62-79. doi: 10.1053/j.gastro.2009.03.035
  2. Ober EA, Lemaigre FP. Development of the liver: Insights into organ and tissue morphogenesis. J Hepatol. 2018;68(5):1049-1062. doi: 10.1016/j.jhep.2018.01.005
  3. Wang X, Yang L, Wang Y-C, et al. Comparative analysis of cell lineage differentiation during hepatogenesis in humans and mice at the single-cell transcriptome level. Cell Res. 2020;30(12):1109-1126. doi: 10.1038/s41422-020-0378-6
  4. Macchi F, Sadler KC. Unraveling the epigenetic basis of liver development, regeneration and disease. Trends Genet. 2020;36(8):587-597. doi: 10.1016/j.tig.2020.05.002
  5. Matchett KP, Wilson-Kanamori JR, Portman JR, et al. Multimodal decoding of human liver regeneration. Nature. 2024;630(8015):158-165. doi: 10.1038/s41586-024-07376-2
  6. Sun T, Pikiolek M, Orsini V, et al. AXIN2<sup>+</sup> Pericentral hepatocytes have limited contributions to liver homeostasis and regeneration. Cell Stem Cell. 2020;26(1):97- 107.e6. doi: 10.1016/j.stem.2019.10.011
  7. Raasch M, Fritsche E, Kurtz A, Bauer M, Mosig AS. Microphysiological systems meet hiPSC technology - new tools for disease modeling of liver infections in basic research and drug development. Adv Drug Deliv Rev. 2019; 140:51-67. doi: 10.1016/j.addr.2018.06.008
  8. Heymann F, Tacke F. Immunology in the liver — from homeostasis to disease. Nat Rev Gastroenterol Hepatol. 2016;13(2):88-110. doi: 10.1038/nrgastro.2015.200
  9. Palakkan AA, Hay DC, PR Anil Kumar, TV Kumary, Ross JA. Liver tissue engineering and cell sources: issues and challenges. Liver Int. 2013;33(5):666-676. doi: 10.1111/liv.12134
  10. Prior N, Inacio P, Huch M. Liver organoids: from basic research to therapeutic applications. Gut. 2019;68(12): 2228-2237. doi: 10.1136/gutjnl-2019-319256
  11. Osonoi S, Takebe T. Organoid-guided precision hepatology for metabolic liver disease. J Hepatol. 2024;80(5): 805-821. doi: 10.1016/j.jhep.2024.01.002
  12. Panwar A, Das P, Tan LP. 3D hepatic organoid-based advancements in LIVER tissue engineering. Bioengineering (Basel). 2021;8(11):185. doi: 10.3390/bioengineering8110185
  13. Yang Z, Liu X, Cribbin EM, Kim AM, Li JJ, Yong KT. Liver-on-a-chip: considerations, advances, and beyond. Biomicrofluidics. 2022;16(6):061502. doi: 10.1063/5.0106855
  14. Dalsbecker P, Beck Adiels C, Goksör M. Liver-on-a-chip devices: the pros and cons of complexity. Am J Physiol Gastrointest Liver Physiol. 2022;323(3):G188-G204. doi: 10.1152/ajpgi.00346.2021
  15. Mirdamadi ES, Kalhori D, Zakeri N, Azarpira N, Solati- Hashjin M. Liver tissue engineering as an emerging alternative for liver disease treatment. Tissue Eng Part B Rev. 2020;26(2):145-163. doi: 10.1089/ten.TEB.2019.0233
  16. Zhang L, Guan Z, Ye JS, Yin YF, Stoltz JF, de Isla N. Research progress in liver tissue engineering. Biomed Mater Eng. 2017;28(s1):S113-s119. doi: 10.3233/bme-171632
  17. Agarwal T, Banerjee D, Konwarh R, et al. Recent advances in bioprinting technologies for engineering hepatic tissue. Mater Sci Eng C Mater Biol Appl. 2021;123:112013. doi: 10.1016/j.msec.2021.112013
  18. Zahra H, Paria P, Polina B, et al. Mimicking the liver function in micro-patterned units: challenges and perspectives in 3D bioprinting. Bioprinting. 2022;27:e00208. doi: 10.1016/j.bprint.2022.e00208
  19. Arka S, Sourabh G. 3D bioprinting strategies for recapitulation of hepatic structure and function in bioengineered liver: a State-of-the-art review. Curr Opin Biomed Eng. 2024;30:100526. doi: 10.1016/j.cobme.2024.100526
  20. Agarwal T, Subramanian B, Maiti TK. Liver tissue engineering: challenges and opportunities. ACS Biomater Sci Eng. 2019;5(9):4167-4182. doi: 10.1021/acsbiomaterials.9b00745
  21. Ordovás L, Park Y, Verfaillie CM. Stem cells and liver engineering. Biotechnol Adv. 2013;31(7):1094-1107. doi: 10.1016/j.biotechadv.2013.07.002
  22. Ali ASM, Wu D, Bannach-Brown A, et al. 3D bioprinting of liver models: a systematic scoping review of methods, bioinks, and reporting quality. Materials Today Bio. 2024;26:100991. doi: 10.1016/j.mtbio.2024.100991
  23. Thompson WL, Takebe T. Human liver model systems in a dish. Dev Growth Differ. 2021;63(1):47-58. doi: 10.1111/dgd.12708
  24. Collardeau-Frachon S, Scoazec J-Y. Vascular development and differentiation during human liver organogenesis. Anat Rec. (Hoboken). 2008;291(6):614-627. doi: 10.1002/ar.20679
  25. Swartley OM, Foley JF, Livingston DP, 3rd, Cullen JM, Elmore SA. Histology atlas of the developing mouse hepatobiliary hemolymphatic vascular system with emphasis on embryonic days 11.5-18.5 and early postnatal development. Toxicol Pathol. 2016;44(5): 705-725. doi: 10.1177/0192623316630836
  26. Zhang H, Pu W, Tian X, et al. Genetic lineage tracing identifies endocardial origin of liver vasculature. Nat Genet. 2016;48(5):537-543. doi: 10.1038/ng.3536
  27. Kang D, Hong G, An S, et al. Bioprinting of multiscaled hepatic lobules within a highly vascularized construct. Small. 2020;16(13):1905505. doi: 10.1002/smll.201905505
  28. Ben-Moshe S, Itzkovitz S. Spatial heterogeneity in the mammalian liver. Nat Rev Gastroenterol Hepatol. 2019;16(7):395-410. doi: 10.1038/s41575-019-0134-x
  29. Gissen P, Arias IM. Structural and functional hepatocyte polarity and liver disease. J Hepatol. 2015;63(4): 1023-1037. doi: 10.1016/j.jhep.2015.06.015
  30. Fu D, Wakabayashi Y, Ido Y, Lippincott-Schwartz J, Arias IM. Regulation of bile canalicular network formation and maintenance by AMP-activated protein kinase and LKB1. J Cell Sci. 2010;123(Pt 19):3294-3302. doi: 10.1242/jcs.068098
  31. Wang T, Yanger K, Stanger BZ, Cassio D, Bi E. Cytokinesis defines a spatial landmark for hepatocyte polarization and apical lumen formation. J Cell Sci. 2014;127(Pt 11): 2483-2492. doi: 10.1242/jcs.139923
  32. Zhang Y, De Mets R, Monzel C, et al. Biomimetic niches reveal the minimal cues to trigger apical lumen formation in single hepatocytes. Nat Mater. 2020;19(9):1026-1035. doi: 10.1038/s41563-020-0662-3
  33. He L, Pu W, Liu X, et al. Proliferation tracing reveals regional hepatocyte generation in liver homeostasis and repair. Science. 2021;371(6532):eabc4346. doi: 10.1126/science.abc4346
  34. Wei Y, Wang YG, Jia Y, et al. Liver homeostasis is maintained by midlobular zone 2 hepatocytes. Science. 2021;371(6532):eabb1625. doi: 10.1126/science.abb1625
  35. MacParland SA, Liu JC, Ma X-Z, et al. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat Commun. 2018;” 9(1):4383. doi: 10.1038/s41467-018-06318-7
  36. He S, Luo Y, Ma W, et al. Endothelial POFUT1 controls injury-induced liver fibrosis by repressing fibrinogen synthesis. J Hepatol. 2024;81(1):135-148. doi: 10.1016/j.jhep.2024.02.032
  37. Shetty S, Lalor PF, Adams DH. Liver sinusoidal endothelial cells — gatekeepers of hepatic immunity. Nat Rev Gastroenterol Hepatol. 2018;15(9):555-567. doi: 10.1038/s41575-018-0020-y
  38. Gracia-Sancho J, Caparrós E, Fernández-Iglesias A, Francés R. Role of liver sinusoidal endothelial cells in liver diseases. Nat Rev Gastroenterol Hepatol. 2021;18(6):411-431. doi: 10.1038/s41575-020-00411-3
  39. Formes H, Bernardes JP, Mann A, et al. The gut microbiota instructs the hepatic endothelial cell transcriptome. iScience. 2021;24(10):103092. doi: 10.1016/j.isci.2021.103092
  40. Banales JM, Huebert RC, Karlsen T, Strazzabosco M, LaRusso NF, Gores GJ. Cholangiocyte pathobiology. Nat Rev Gastroenterol Hepatol. 2019;16(5):269-281. doi: 10.1038/s41575-019-0125-y
  41. Tabibian JH, Masyuk AI, Masyuk TV, O’Hara SP, LaRusso NF. Physiology of cholangiocytes. Compr Physiol. 2013;3(1): 541-565. doi: 10.1002/cphy.c120019
  42. Cervantes-Alvarez E, Wang Y, Collin de l’Hortet A, Guzman- Lepe J, Zhu J, Takeishi K. Current strategies to generate mature human induced pluripotent stem cells derived cholangiocytes and future applications. Organogenesis. 2017;13(1):1-15. doi: 10.1080/15476278.2016.1278133
  43. Sampaziotis F, Cardoso de Brito M, Madrigal P, et al. Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation. Nat Biotechnol. 2015;33(8):845-852. doi: 10.1038/nbt.3275
  44. Ogawa M, Jiang J-X, Xia S, et al. Generation of functional ciliated cholangiocytes from human pluripotent stem cells. Nat Commun. 2021;12(1):6504. doi: 10.1038/s41467-021-26764-0
  45. Kamm DR, McCommis KS. Hepatic stellate cells in physiology and pathology. J Physiol. 2022;600(8): 1825-1837. doi: 10.1113/jp281061
  46. Tsuchida T, Friedman SL. Mechanisms of hepatic stellate cell activation. Nat Rev Gastroenterol Hepatol. 2017;14(7): 397-411. doi: 10.1038/nrgastro.2017.38
  47. Krenkel O, Tacke F. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol. 2017;17(5):306-321. doi: 10.1038/nri.2017.11
  48. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol. 2009;9(4):259-270. doi: 10.1038/nri2528
  49. Zong Y, Stanger BZ. Molecular mechanisms of liver and bile duct development. Wiley Interdiscip Rev Dev Biol. 2012;1(5):643-655. doi: 10.1002/wdev.47
  50. Si-Tayeb K, Lemaigre FP, Duncan SA. Organogenesis and development of the liver. Dev Cell. 2010;18(2):175-189. doi: 10.1016/j.devcel.2010.01.011
  51. Gordillo M, Evans T, Gouon-Evans V. Orchestrating liver development. Development. 2015;142(12):2094-2108. doi: 10.1242/dev.114215
  52. Yang L, Li L-C, Lamaoqiezhong, et al. The contributions of mesoderm-derived cells in liver development. Semin Cell Dev Biol. 2019;92:63-76. doi: 10.1016/j.semcdb.2018.09.003
  53. Liang Y, Kaneko K, Xin B, et al. Temporal analyses of postnatal liver development and maturation by single-cell transcriptomics. Dev Cell. 2022;57(3):398-414.e5. doi: 10.1016/j.devcel.2022.01.004
  54. Alison M, Islam S, Lim S. Stem cells in liver regeneration, fibrosis and cancer: the good, the bad and the ugly. J Pathol. 2009;217(2):282-298. doi: 10.1002/path.2453
  55. Miyajima A, Tanaka M, Itoh T. Stem/Progenitor cells in liver development, homeostasis, regeneration, and reprogramming. Cell Stem Cell. 2014;14(5):561-574. doi: 10.1016/j.stem.2014.04.010
  56. Michalopoulos GK. Liver regeneration. J Cell Physiol. 2007;213(2):286-300. doi: 10.1002/jcp.21172
  57. Miyaoka Y, Ebato K, Kato H, Arakawa S, Shimizu S, Miyajima A. Hypertrophy and unconventional cell division of hepatocytes underlie liver regeneration. Curr Biol. 2012;22(13):1166-1175. doi: 10.1016/j.cub.2012.05.016
  58. Devarbhavi H, Asrani SK, Arab JP, Nartey YA, Pose E, Kamath PS. Global burden of liver disease: 2023 update. J Hepatol. 2023;79(2):516-537. doi: 10.1016/j.jhep.2023.03.017
  59. Bhatia SN, Underhill GH, Zaret KS, Fox IJ. Cell and tissue engineering for liver disease. Sci Transl Med. 2014;6(245):245sr2. doi: 10.1126/scitranslmed.3005975
  60. Sun Y, Chang J, Liu X, Liu C. Mortality trends of liver diseases in mainland China over three decades: an age-period-cohort analysis. BMJ Open. 2019;9(11):e029793. doi: 10.1136/bmjopen-2019-029793
  61. Mohiuddin MM, Singh AK, Scobie L, et al. Graft dysfunction in compassionate use of genetically engineered pig-to-human cardiac xenotransplantation: a case report. Lancet. 2023;402(10399):397-410. doi: 10.1016/S0140-6736(23)00775-4
  62. Mallapaty S, Kozlov M. First pig kidney transplant in a person: what it means for the future. Nature. 2024;628(8006):13-14. doi: 10.1038/d41586-024-00879-y
  63. Sun Z, Yuan X, Wu J, et al. Hepatocyte transplantation: the progress and the challenges. Hepatol Commun. 2023;7(10):e0266. doi: 10.1097/hc9.0000000000000266
  64. Struecker B, Raschzok N, Sauer IM. Liver support strategies: cutting-edge technologies. Nat Rev Gastroenterol Hepatol. 2014;11(3):166-176. doi: 10.1038/nrgastro.2013.204
  65. Millis JM, Losanoff JE. Technology Insight: liver support systems. Nat Clin Pract Gastroenterol Hepatol. 2005;2(9): 398-405. doi: 10.1038/ncpgasthep0254
  66. Krisper P, Stauber RE. Technology insight: artificial extracorporeal liver support—how does Prometheus® compare with MARS®? Nat Clin Pract Nephrol. 2007;3(5): 267-276. doi: 10.1038/ncpneph0466
  67. Strain AJ, Neuberger JM. A bioartificial liver--state of the art. Science. 2002;295(5557):1005-1009. doi: 10.1126/science.1068660
  68. Glorioso JM, Mao SA, Rodysill B, et al. Pivotal preclinical trial of the spheroid reservoir bioartificial liver. J Hepatol. 2015;63(2):388-398. doi: 10.1016/j.jhep.2015.03.021
  69. Li Y, Wu Q, Wang Y, et al. Novel spheroid reservoir bioartificial liver improves survival of nonhuman primates in a toxin-induced model of acute liver failure. Theranostics. 2018;8(20):5562-5574. doi: 10.7150/thno.26540
  70. Thompson J, Jones N, Al‐Khafaji A, et al. Extracorporeal cellular therapy (ELAD) in severe alcoholic hepatitis: a multinational, prospective, controlled, randomized trial. Liver Transpl. 2018;24(3):380-393. doi: 10.1002/lt.24986
  71. Chen S, Wang J, Ren H, et al. Hepatic spheroids derived from human induced pluripotent stem cells in bio-artificial liver rescue porcine acute liver failure. Cell Res. 2020; 30(1):95-97. doi: 10.1038/s41422-019-0261-5
  72. Li W-J, Zhu X-J, Yuan T-J, et al. An extracorporeal bioartificial liver embedded with 3D-layered human liver progenitor-like cells relieves acute liver failure in pigs. Sci Transl Med. 2020;12(551):eaba5146. doi: 10.1126/scitranslmed.aba5146
  73. Wang Y, Zheng Q, Sun Z, et al. Reversal of liver failure using a bioartificial liver device implanted with clinical-grade human-induced hepatocytes. Cell Stem Cell. 2023;30(5):617- 631.e8. doi: 10.1016/j.stem.2023.03.013
  74. Shi X-L, Gao Y, Yan Y, et al. Improved survival of porcine acute liver failure by a bioartificial liver device implanted with induced human functional hepatocytes. Cell Res. 2016;26(2):206-216. doi: 10.1038/cr.2016.6
  75. Hofer M, Lutolf MP. Engineering organoids. Nat Rev Mater. 2021;6(5):402-420. doi: 10.1038/s41578-021-00279-y
  76. Zhao Z, Chen X, Dowbaj AM, et al. Organoids. Nat Rev Methods Primers. 2022;2(1):94. doi: 10.1038/s43586-022-00174-y
  77. Rossi G, Manfrin A, Lutolf MP. Progress and potential in organoid research. Nat Rev Genet. 2018;19(11):671-687. doi: 10.1038/s41576-018-0051-9
  78. Harrison SP, Baumgarten SF, Verma R, Lunov O, Dejneka A, Sullivan GJ. Liver organoids: recent developments, limitations and potential. Front Med (Lausanne). 2021;8:574047. doi: 10.3389/fmed.2021.574047
  79. Hu H, Gehart H, Artegiani B, et al. Long-term expansion of functional mouse and human hepatocytes as 3D organoids. Cell. 2018;175(6):1591-1606.e19. doi: 10.1016/j.cell.2018.11.013
  80. Huch M, Dorrell C, Boj SF, et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature. 2013;494(7436):247-250. doi: 10.1038/nature11826
  81. Huch M, Gehart H, van Boxtel R, et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell. 2015;160(1):299-312. doi: 10.1016/j.cell.2014.11.050
  82. Vyas D, Baptista PM, Brovold M, et al. Self‐assembled liver organoids recapitulate hepatobiliary organogenesis in vitro. Hepatology. 2018;67(2):750-761. doi: 10.1002/hep.29483
  83. Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature. 2013;499(7459):481-484. doi: 10.1038/nature12271
  84. Wu F, Wu D, Ren Y, et al. Generation of hepatobiliary organoids from human induced pluripotent stem cells. J Hepatol. 2019;70(6):1145-1158. doi: 10.1016/j.jhep.2018.12.028
  85. Sorrentino G, Rezakhani S, Yildiz E, et al. Mechano-modulatory synthetic niches for liver organoid derivation. Nat Commun. 2020;11(1):3416. doi: 10.1038/s41467-020-17161-0
  86. Zhang S, Xu G, Wu J, et al. Microphysiological constructs and systems: biofabrication tactics, biomimetic evaluation approaches, and biomedical applications. Small Methods. 2024;8(1):2300685. doi: 10.1002/smtd.202300685
  87. Zhang B, Korolj A, Lai BFL, Radisic M. Advances in organ-on-a-chip engineering. Nat Rev Mater. 2018;3(8):257-278. doi: 10.1038/s41578-018-0034-7
  88. 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
  89. 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
  90. 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
  91. Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol. 2014;32(8):760-772. doi: 10.1038/nbt.2989
  92. Moradi E, Jalili-Firoozinezhad S, Solati-Hashjin M. Microfluidic organ-on-a-chip models of human liver tissue. Acta Biomater. 2020;116:67-83. doi: 10.1016/j.actbio.2020.08.041
  93. 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
  94. Siwczak F, Cseresnyes Z, Hassan MIA, et al. Human macrophage polarization determines bacterial persistence of Staphylococcus aureus in a liver-on-chip-based infection model. Biomaterials. 2022;287:121632. doi: 10.1016/j.biomaterials.2022.121632
  95. Jang K-J, Otieno MA, Ronxhi J, et al. Reproducing human and cross-species drug toxicities using a Liver-Chip. Sci Transl Med. 2019;11(517):eaax5516. doi: 10.1126/scitranslmed.aax5516
  96. Nawroth JC, Petropolis DB, Manatakis DV, et al. Modeling alcohol-associated liver disease in a human Liver-Chip. Cell Rep. 2021;36(3):109393. doi: 10.1016/j.celrep.2021.109393
  97. Ewart L, Apostolou A, Briggs SA, et al. Performance assessment and economic analysis of a human Liver-Chip for predictive toxicology. Commun Med. 2022;2(1):154. doi: 10.1038/s43856-022-00209-1
  98. Du K, Li S, Li C, et al. Modeling nonalcoholic fatty liver disease on a liver lobule chip with dual blood supply. Acta Biomater. 2021;134:228-239. doi: 10.1016/j.actbio.2021.07.013
  99. Hong G, Kim J, Oh H, et al. Production of multiple cell-laden microtissue spheroids with a biomimetic hepatic-lobule-like structure. Adv Mater. 2021;33(36):2102624. doi: 10.1002/adma.202102624
  100. Vunjak-Novakovic G, Ronaldson-Bouchard K, Radisic M. Organs-on-a-chip models for biological research. Cell. 2021;184(18):4597-4611. doi: 10.1016/j.cell.2021.08.005
  101. Ehrlich A, Duche D, Ouedraogo G, Nahmias Y. Challenges and opportunities in the design of liver-on-chip microdevices. Annu Rev Biomed Eng. 2019;21:219-239. doi: 10.1146/annurev-bioeng-060418-052305
  102. Moroni L, Burdick JA, Highley C, et al. Biofabrication strategies for 3D in vitro models and regenerative medicine. Nat Rev Mater. 2018;3(5):21-37. doi: 10.1038/s41578-018-0006-y
  103. Daly AC, Prendergast ME, Hughes AJ, Burdick JA. Bioprinting for the biologist. Cell. 2021;184(1):18-32. doi: 10.1016/j.cell.2020.12.002
  104. Morgan FLC, Moroni L, Baker MB. Dynamic bioinks to advance bioprinting. Adv Healthcare Mater. 2020;9(15):1901798. doi: 10.1002/adhm.201901798
  105. Chimene D, Lennox KK, Kaunas RR, Gaharwar AK. Advanced bioinks for 3D printing: a materials science perspective. Ann Biomed Eng. 2016;44(6):2090-2102. doi: 10.1007/s10439-016-1638-y
  106. Heinrich MA, Liu W, Jimenez A, et al. 3D bioprinting: from benches to translational applications. Small. 2019;15(23):1805510. doi: 10.1002/smll.201805510
  107. 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
  108. Lou J, Mooney DJ. Chemical strategies to engineer hydrogels for cell culture. Nat Rev Chem. 2022;6(10):726-744. doi: 10.1038/s41570-022-00420-7
  109. Chaudhuri O, Cooper-White J, Janmey PA, Mooney DJ, Shenoy VB. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature. 2020;584(7822): 535-546. doi: 10.1038/s41586-020-2612-2
  110. Rizwan M, Ling C, Guo C, et al. Viscoelastic notch signaling hydrogel induces liver bile duct organoid growth and morphogenesis. Adv Healthc Mater. 2022; 11(23):2200880. doi: 10.1002/adhm.202200880
  111. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773-785. doi: 10.1038/nbt.2958
  112. Vasconcelos DP, Águas AP, Barbosa MA, Pelegrín P, Barbosa JN. The inflammasome in host response to biomaterials: bridging inflammation and tissue regeneration. Acta Biomater. 2019;83:1-12. doi: 10.1016/j.actbio.2018.09.056
  113. Levato R, Jungst T, Scheuring RG, Blunk T, Groll J, Malda J. From shape to function: the next step in bioprinting. Adv Mater. 2020;32(12):1906423. doi: 10.1002/adma.201906423
  114. Wang Y, Cui C-B, Yamauchi M, et al. Lineage restriction of human hepatic stem cells to mature fates is made efficient by tissue-specific biomatrix scaffolds. Hepatology. 2011;53(1):293-305. doi: 10.1002/hep.24012
  115. 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
  116. Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol. 2014;15(12):771-785. doi: 10.1038/nrm3902
  117. Donderwinkel I, van Hest JCM, Cameron NR. Bio-inks for 3D bioprinting: recent advances and future prospects. Polymer Chem. 2017;8(31):4451-4471. doi: 10.1039/C7PY00826K
  118. 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
  119. Reizabal A, Costa CM, Pérez-Álvarez L, Vilas-Vilela JL, Lanceros-Méndez S. Silk fibroin as sustainable advanced material: material properties and characteristics, processing, and applications. Adv Funct Mater. 2023;33(3):2210764. doi: 10.1002/adfm.202210764
  120. Maity C, Das N. Alginate-based smart materials and their application: recent advances and perspectives. Top Curr Chem (Cham). 2021;380(1):3. doi: 10.1007/s41061-021-00360-8
  121. Spearman BS, Agrawal NK, Rubiano A, Simmons CS, Mobini S, Schmidt CE. Tunable methacrylated hyaluronic acid-based hydrogels as scaffolds for soft tissue engineering applications. J Biomed Mater Res A. 2020;108(2):279-291. doi: 10.1002/jbm.a.36814
  122. Ma X, Qu X, Zhu W, et al. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc Natl Acad Sci U S A. 2016;113(8): 2206-2211. doi: 10.1073/pnas.1524510113
  123. Baier Leach J, Bivens KA, Patrick CW, Jr., Schmidt CE. Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng. 2003;82(5):578-589. doi: 10.1002/bit.10605
  124. Zarrintaj P, Manouchehri S, Ahmadi Z, et al. Agarose-based biomaterials for tissue engineering. Carbohydr Polym. 2018;187:66-84. doi: 10.1016/j.carbpol.2018.01.060
  125. López-Marcial GR, Zeng AY, Osuna C, Dennis J, García JM, O’Connell GD. Agarose-based hydrogels as suitable bioprinting materials for tissue engineering. ACS Biomater Sci Eng. 2018;4(10):3610-3616. doi: 10.1021/acsbiomaterials.8b00903
  126. Hasebe Y, Okumura N, Koh T, et al. Formation of rat hepatocyte spheroids on agarose. Hepatol Res. 2005;32(2): 89-95. doi: 10.1016/j.hepres.2005.03.012
  127. Passaniti A, Kleinman HK, Martin GR. Matrigel: history/ background, uses, and future applications. J Cell Commun Signal. 2022;16(4):621-626. doi: 10.1007/s12079-021-00643-1
  128. Jiang S, Zhuang Y, Cai M, Wang X, Lin K. Decellularized extracellular matrix: a promising strategy for skin repair and regeneration. Eng Regenerat. 2023;4(4):357-374. doi: 10.1016/j.engreg.2023.05.001
  129. Deng B, Ma Y, Huang J, et al. Revitalizing liver function in mice with liver failure through transplantation of 3D-bioprinted liver with expanded primary hepatocytes. Sci Adv. 2024;10(23):eado1550. doi: 10.1126/sciadv.ado1550
  130. Lutolf MP, Lauer-Fields JL, Schmoekel HG, et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci U S A. 2003;100(9): 5413-5418. doi: 10.1073/pnas.0737381100
  131. Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci U S A. 2016;113(12):3179-3184. doi: 10.1073/pnas.1521342113
  132. Gu Q, Tomaskovic-Crook E, Wallace GG, Crook JM. 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv Healthc Mater. 2017;6(17):1700175. doi: 10.1002/adhm.201700175
  133. Andersson TB, Kanebratt KP, Kenna JG. The HepaRG cell line: a unique in vitro tool for understanding drug metabolism and toxicology in human. Expert Opin Drug Metab Toxicol. 2012;8(7):909-920. doi: 10.1517/17425255.2012.685159
  134. Cerec V, Glaise D, Garnier D, et al. Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology. 2007;45(4):957-967. doi: 10.1002/hep.21536
  135. Gripon P, Rumin S, Urban S, et al. Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci U S A. 2002;99(24):15655-15660. doi: 10.1073/pnas.232137699
  136. Higuchi Y, Kawai K, Yamazaki H, et al. The human hepatic cell line HepaRG as a possible cell source for the generation of humanized liver TK-NOG mice. Xenobiotica. 2014;44(2):146-153. doi: 10.3109/00498254.2013.836257
  137. Laurent V, Glaise D, Nübel T, Gilot D, Corlu A, Loyer P. Highly efficient SiRNA and gene transfer into hepatocyte-like HepaRG cells and primary human hepatocytes: new means for drug metabolism and toxicity studies. Methods Mol Biol. 2013;987:295-314. doi: 10.1007/978-1-62703-321-3_25
  138. Koike H, Iwasawa K, Ouchi R, et al. Engineering human hepato-biliary-pancreatic organoids from pluripotent stem cells. Nat Protoc. 2021;16(2):919-936. doi: 10.1038/s41596-020-00441-w
  139. Koike H, Iwasawa K, Ouchi R, et al. Modelling human hepato-biliary-pancreatic organogenesis from the foregut-midgut boundary. Nature. 2019;574(7776):112-116. doi: 10.1038/s41586-019-1598-0
  140. Hannan NR, Segeritz CP, Touboul T, Vallier L. Production of hepatocyte-like cells from human pluripotent stem cells. Nat Protoc. 2013;8(2):430-437. doi: 10.1038/nprot.2012.153
  141. Dao Thi VL, Wu X, Belote RL, et al. Stem cell-derived polarized hepatocytes. Nat Commun. 2020;11(1):1677. doi: 10.1038/s41467-020-15337-2
  142. Lee H, Chae S, Kim JY, et al. Cell-printed 3D liver-on-a-chip possessing a liver microenvironment and biliary system. Biofabrication. 2019;11(2):025001. doi: 10.1088/1758-5090/aaf9fa
  143. Liu Q, Mille LS, Villalobos C, et al. 3D-bioprinted cholangiocarcinoma-on-a-chip model for evaluating drug responses. Bio-Design Manuf. 2023;6(4):373-389. doi: 10.1007/s42242-022-00229-9
  144. Hafiz EOA, Bulutoglu B, Mansy SS, et al. Development of liver microtissues with functional biliary ductular network. Biotechnol Bioeng. 2021;118(1):17-29. doi: 10.1002/bit.27546
  145. Stevens KR, Scull MA, Ramanan V, et al. In situ expansion of engineered human liver tissue in a mouse model of chronic liver disease. Sci Transl Med. 2017;9(399):eaah5505. doi: 10.1126/scitranslmed.aah5505
  146. Grigoryan B, Paulsen SJ, Corbett DC, et al. Multivascular networks and functional intravascular topologies within biocompatible hydrogels. Science. 2019;364(6439): 458-464. doi: 10.1126/science.aav9750
  147. Peng X, Janićijević Ž, Lemm S, et al. Impact of viscosity on human hepatoma spheroids in soft core–shell microcapsules. Adv Healthc Mater. 2024;13(11):2302609. doi: 10.1002/adhm.202302609
  148. Foyt DA, Norman MDA, Yu TTL, Gentleman E. Exploiting advanced hydrogel technologies to address key challenges in regenerative medicine. Adv Healthc Mater. 2018;7(8):1700939. doi: 10.1002/adhm.201700939
  149. Bishop ES, Mostafa S, Pakvasa M, et al. 3-D bioprinting technologies in tissue engineering and regenerative medicine: current and future trends. Genes Dis. 2017;4(4):185-195. doi: 10.1016/j.gendis.2017.10.002
  150. Xu C, Zhang M, Huang Y, Ogale A, Fu J, Markwald RR. Study of droplet formation process during drop-on-demand inkjetting of living cell-Laden Bioink. Langmuir. 2014;30(30):9130-9138. doi: 10.1021/la501430x
  151. Matsusaki M, Sakaue K, Kadowaki K, Akashi M. Three-dimensional human tissue chips fabricated by rapid and automatic inkjet cell printing. Adv Healthc Mater. 2013;2(4):534-539. doi: 10.1002/adhm.201200299
  152. Jian H, Li X, Dong Q, Tian S, Bai S. In vitro construction of liver organoids with biomimetic lobule structure by a multicellular 3D bioprinting strategy. Cell Prolif. 2023;56(5):e13465. doi: 10.1111/cpr.13465
  153. Gu Z, Fu J, Lin H, He Y. Development of 3D bioprinting: from printing methods to biomedical applications. Asian J Pharm Sci. 2020;15(5):529-557. doi: 10.1016/j.ajps.2019.11.003
  154. Dou C, Perez V, Qu J, Tsin A, Xu B, Li J. A State-of-the-Art review of laser-assisted bioprinting and its future research trends. ChemBioEng Rev. 2021;8(5):517-534. doi: 10.1002/cben.202000037
  155. Zhu W, Qu X, Zhu J, et al. Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials. 2017;124:106-115. doi: 10.1016/j.biomaterials.2017.01.042
  156. Wang M, Li W, Hao J, et al. Molecularly cleavable bioinks facilitate high-performance digital light processing-based bioprinting of functional volumetric soft tissues. Nat Commun. 2022;13(1):3317. doi: 10.1038/s41467-022-31002-2
  157. Jing S, Lian L, Hou Y, et al. Advances in volumetric bioprinting. Biofabrication. 2024;16(1):012004. doi: 10.1088/1758-5090/ad0978
  158. Bernal PN, Bouwmeester M, Madrid-Wolff J, et al. Volumetric bioprinting of organoids and optically tuned hydrogels to build liver-like metabolic biofactories. Adv Mater. 2022;34(15):2110054. doi: 10.1002/adma.202110054
  159. Miller JS, Stevens KR, Yang MT, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater. 2012;11(9):768-774. doi: 10.1038/nmat3357
  160. Liu X, Wang X, Zhang L, et al. 3D liver tissue model with branched vascular networks by multimaterial bioprinting. Adv Healthc Mater. 2021;10(23):2101405. doi: 10.1002/adhm.202101405
  161. Yang H, Sun L, Pang Y, et al. Three-dimensional bioprinted hepatorganoids prolong survival of mice with liver failure. Gut. 2021;70(3):567-574. doi: 10.1136/gutjnl-2019-319960
  162. McCormack A, Highley CB, Leslie NR, Melchels FPW. 3D printing in suspension baths: keeping the promises of bioprinting afloat. Trends Biotechnol. 2020;38(6):584-593. doi: 10.1016/j.tibtech.2019.12.020
  163. Lee A, Hudson AR, Shiwarski DJ, et al. 3D bioprinting of collagen to rebuild components of the human heart. Science. 2019;365(6452):482-487. doi: 10.1126/science.aav9051
  164. Hinton TJ, Jallerat Q, Palchesko RN, et al. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv. 2015;1(9):e1500758. doi: 10.1126/sciadv.1500758
  165. Fang Y, Ji M, Yang Y, et al. 3D printing of vascularized hepatic tissues with a high cell density and heterogeneous microenvironment. Biofabrication. 2023;15(4):045004. doi: 10.1088/1758-5090/ace5e0
  166. Taymour R, Chicaiza-Cabezas NA, Gelinsky M, Lode A. Core–shell bioprinting of vascularized in vitro liver sinusoid models. Biofabrication. 2022;14(4):045019. doi: 10.1088/1758-5090/ac9019
  167. Wang H, Liu X, Gu Q, Zheng X. Vascularized organ bioprinting: from strategy to paradigm. Cell Prolif. 2023;56(5):e13453. doi: 10.1111/cpr.13453
  168. Kinstlinger IS, Saxton SH, Calderon GA, et al. Generation of model tissues with dendritic vascular networks via sacrificial laser-sintered carbohydrate templates. Nat Biomed Eng. 2020;4(9):916-932. doi: 10.1038/s41551-020-0566-1
  169. O’Connor C, Brady E, Zheng Y, Moore E, Stevens KR. Engineering the multiscale complexity of vascular networks. Nat Rev Mater. 2022;7(9):702-716. doi: 10.1038/s41578-022-00447-8
  170. Zong Y, Stanger BZ. Molecular mechanisms of bile duct development. Int J Biochem Cell Biol. 2011;43(2): 257-264. doi: 10.1016/j.biocel.2010.06.020
  171. Raynaud P, Carpentier R, Antoniou A, Lemaigre FP. Biliary differentiation and bile duct morphogenesis in development and disease. Int J Biochem Cell Biol. 2011;43(2): 245-256. doi: 10.1016/j.biocel.2009.07.020
  172. Justin AW, Saeb-Parsy K, Markaki AE, Vallier L, Sampaziotis F. Advances in the generation of bioengineered bile ducts. Biochim Biophys Acta Mol Basis Dis. 2018;1864(4PtB): 1532-1538. doi: 10.1016/j.bbadis.2017.10.034
  173. Wang Z, Faria J, Penning LC, Masereeuw R, Spee B. Tissue-engineered bile ducts for disease modeling and therapy. Tissue Eng Part C Methods. 2021;27(2):59-76. doi: 10.1089/ten.TEC.2020.0283
  174. Squires RH, Ng V, Romero R, et al. Evaluation of the pediatric patient for liver transplantation. J Pediatr Gastroenterol Nutr. 2014;59(1):112-131. doi: 10.1097/MPG.0000000000000431
  175. Brevini T, Tysoe OC, Sampaziotis F. Tissue engineering of the biliary tract and modelling of cholestatic disorders. J Hepatol. 2020;73(4):918-932. doi: 10.1016/j.jhep.2020.05.049
  176. Sun Q, Shen Z, Liang X, et al. Progress and current limitations of materials for artificial bile duct engineering. Materials. 2021;14(23):7468. doi: 10.3390/ma14237468
  177. Lewis PL, Su J, Yan M, et al. Complex bile duct network formation within liver decellularized extracellular matrix hydrogels. Sci Rep. 2018;8(1):12220. doi: 10.1038/s41598-018-30433-6
  178. Sampaziotis F, Muraro D, Tysoe OC, et al. Cholangiocyte organoids can repair bile ducts after transplantation in the human liver. Science. 2021;371(6531):839-846. doi: 10.1126/science.aaz6964
  179. Sampaziotis F, Justin AW, Tysoe OC, et al. Reconstruction of the mouse extrahepatic biliary tree using primary human extrahepatic cholangiocyte organoids. Nat Med. 2017;23(8):954-963. doi: 10.1038/nm.4360
  180. Roos FJM, van Tienderen GS, Wu H, et al. Human branching cholangiocyte organoids recapitulate functional bile duct formation. Cell Stem Cell. 2022;29(5):776-794.e13. doi: 10.1016/j.stem.2022.04.011
  181. Du Y, de Jong IEM, Gupta K, et al. Human vascularized bile duct-on-a chip: a multi-cellular micro-physiological system for studying cholestatic liver disease. Biofabrication. 2023;16(1):015004. doi: 10.1088/1758-5090/ad0261
  182. Du Y, Khandekar G, Llewellyn J, Polacheck W, Chen CS, Wells RG. A bile duct-on-a-chip with organ-level functions. Hepatology. 2020;71(4):1350-1363. doi: 10.1002/hep.30918
  183. Tanimizu N, Ichinohe N, Sasaki Y, et al. Generation of functional liver organoids on combining hepatocytes and cholangiocytes with hepatobiliary connections ex vivo. Nature Commun. 2021;12(1):3390. doi: 10.1038/s41467-021-23575-1
  184. Loterie D, Delrot P, Moser C. High-resolution tomographic volumetric additive manufacturing. Nat Commun. 2020;11(1):852. doi: 10.1038/s41467-020-14630-4
  185. Kelly BE, Bhattacharya I, Heidari H, Shusteff M, Spadaccini CM, Taylor HK. Volumetric additive manufacturing via tomographic reconstruction. Science. 2019;363(6431): 1075-1079. doi: 10.1126/science.aau7114
  186. Bernal PN, Delrot P, Loterie D, et al. Volumetric bioprinting of complex living-tissue constructs within seconds. Adv Mater. 2019;31(42):e1904209. doi: 10.1002/adma.201904209
  187. Cai H, Wu Z, Ao Z, et al. Trapping cell spheroids and organoids using digital acoustofluidics. Biofabrication. 2020;12(3):035025. doi: 10.1088/1758-5090/ab9582
  188. Johnson K, Melchert D, Gianola DS, Begley M, Ray TR. Recent progress in acoustic field-assisted 3D-printing of functional composite materials. MRS Adv. 2021;6(25): 636-643. doi: 10.1557/s43580-021-00090-5
  189. Foresti D, Kroll KT, Amissah R, et al. Acoustophoretic printing. Sci Adv. 2018;4(8):eaat1659. doi: 10.1126/sciadv.aat1659
  190. Jentsch S, Nasehi R, Kuckelkorn C, Gundert B, Aveic S, Fischer H. Multiscale 3D bioprinting by nozzle-free acoustic droplet ejection. Small Methods. 2021;5(6):2000971. doi: 10.1002/smtd.202000971
  191. Guo Q, Su X, Zhang X, Shao M, Yu H, Li D. A review on acoustic droplet ejection technology and system. Soft Matter. 2021;17(11):3010-3021. doi: 10.1039/D0SM02193H
  192. Liu C, Pandit PP, Parsons C, Khan F, Hu Y. Acoustic field-assisted inkjet-based additive manufacturing of carbon fiber-reinforced polydimethylsiloxane composites. J Manuf Process. 2022;80:87-94. doi: 10.1016/j.jmapro.2022.05.059
  193. Wadsworth P, Nelson I, Porter DL, Raeymaekers B, Naleway SE. Manufacturing bioinspired flexible materials using ultrasound directed self-assembly and 3D printing. Mater Design. 2020;185:108243. doi: 10.1016/j.matdes.2019.108243
  194. Chen K, Jiang E, Wei X, et al. The acoustic droplet printing of functional tumor microenvironments. Lab Chip. 2021;21(8):1604-1612. doi: 10.1039/D1LC00003A
  195. Lei Y, Hu H. SAW-driven droplet jetting technology in microfluidic: a review. Biomicrofluidics. 2020;14(6): 061505. doi: 10.1063/5.0014768
  196. Kim SH, Seo YB, Yeon YK, et al. 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials. 2020;260: 120281. doi: 10.1016/j.biomaterials.2020.120281
  197. Li K, Huang W, Guo H, et al. Advancements in robotic arm-based 3D bioprinting for biomedical applications. Life Med. 2023;2(6):lnad046 doi: 10.1093/lifemedi/lnad046
  198. An J, Zhang S, Wu J, et al. Assessing bioartificial organ function: the 3P model framework and its validation. Lab Chip. 2024;24(6):1586-1601. doi: 10.1039/D3LC01020A



 

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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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