Organ mimicking technologies and their applications in drug discovery

Yueyang Qu, Jiaming Ye, Bingcheng Lin, Yong Luo, Xiuli Zhang

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Intelligent Pharmacy ›› 2023, Vol. 1 ›› Issue (2) : 73-89. DOI: 10.1016/j.ipha.2023.05.003

Organ mimicking technologies and their applications in drug discovery

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Abstract

The significant gap between animal experimentation and clinical trials has resulted in immense expenses in time and money in drug development. The popularity of researches on alternative models to animal experimentation has grown, with the development of artificial organs at its forefront. Three state-of-the-art technologies used to simulate organs are organ-on-a-chip, organoid, and 3D bioprinting. Organ-on-a-chip technology utilizes flexible fluidic manipulation and accurate recreation of the cell microenvironment. Organoid technology allows for the development of personalized mini-organs and the testing of drugs on different human species. 3D bioprinting technology is capable of creating artificial organs with intricate 3D structures. All these technologies play a significant role in developing drugs in highly efficient mode.

Keywords

Drug discovery / Organ-on-a-chip / Organoid / 3D bioprinting / Microphysiological system

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Yueyang Qu, Jiaming Ye, Bingcheng Lin, Yong Luo, Xiuli Zhang. Organ mimicking technologies and their applications in drug discovery. Intelligent Pharmacy, 2023, 1(2): 73‒89 https://doi.org/10.1016/j.ipha.2023.05.003

References

[1]
Zhang B, Korolj A, Lai BFL, et al. Advances in organ-on-a-chip engineering. Nat Rev Mater. 2018;3(8):257–278.https://doi.org/10.1038/s41578-018-0034-7.
[2]
Kim J, Koo BK, Knoblich JA. Human organoids: model systems for human biology and medicine. Nat Rev Mol Cell Biol. 2020;21(10):571–584.https://doi.org/10.1038/s41580-020-0259-3.
[3]
Bang S, Lee S, Choi N, et al. Emerging brain-pathophysiology-mimetic platforms for studying neurodegenerative diseases: brain organoids and brains-on-a-chip. Adv Healthcare Mater. 2021;10(12), 2002119.https://doi.org/10.1002/adhm.202002119.
[4]
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. https://doi.org/10.3390/mi10100676.
[5]
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.https://doi.org/10.1038/s41592-019-0325-y.
[6]
Shik Mun K, Arora K, Huang Y, et al. Patient-derived pancreas-on-a-chip to model cystic fibrosis-related disorders. Nat Commun. 2019;10(1):3124.https://doi.org/10.1038/s41467-019-11178-w.
[7]
Jalili-Firoozinezhad S, Gazzaniga FS, Calamari EL, et al. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat Biomed Eng. 2019; 3(7):520–531.https://doi.org/10.1038/s41551-019-0397-0.
[8]
Fu Z, Ouyang L, Xu R, et al. Responsive biomaterials for 3d bioprinting: a review. Mater Today. 2022; 52: 112- 132. https://doi.org/10.1016/j.mattod.2022.01.001.
[9]
Slaughter VL, Rumsey JW, Boone R, et al. Validation of an adipose-liver human-ona-chip model of nafld for preclinical therapeutic efficacy evaluation. Sci Rep. 2021; 11(1):1–10.https://doi.org/10.1038/s41598-021-92264-2.
[10]
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. https://doi.org/10.1016/j.actbio.2021.07.013.
[11]
Jang KJ, Otieno MA, Ronxhi J, et al. Reproducing human and cross-species drug toxicities using a liver-chip. Sci Transl Med. 2019; 11 (517): x5516. https://doi.org/10.1126/scitranslmed.aax5516.
[12]
Nawroth JC, Petropolis DB, Manatakis DV, et al. Modeling alcohol-associated liver disease in a human liver-chip. Cell Rep. 2021;36(3), 109393.https://doi.org/10.1016/j.celrep.2021.109393.
[13]
Deng J, Zhang X, Chen Z, et al. A cell lines derived microfluidic liver model for investigation of hepatotoxicity induced by drug-drug interaction. Biomicrofluidics. 2019;13(2), 24101.https://doi.org/10.1063/1.5070088.
[14]
Tian T, Ho Y, Chen C, et al. A 3d bio-printed spheroids based perfusion in vitro liver on chip for drug toxicity assays. Chin Chem Lett. 2022; 33 (6): 3167- 3171. https://doi.org/10.1016/j.cclet.2021.11.029.
[15]
Nieskens TTG, Persson M, Kelly EJ, et al. A multicompartment human kidney proximal tubule-on-a-chip replicates cell polarization-dependent cisplatin toxicity. Drug Metabol Dispos. 2020; 48 (12): 1303- 1311. https://doi.org/10.1124/dmd.120.000098.
[16]
Jansen J, Jansen K, Neven E, et al. Remote sensing and signaling in kidney proximal tubules stimulates gut microbiome-derived organic anion secretion. In: Proceedings of the National Academy of Sciences. vol. 116. 2019:16105–16110.https://doi.org/10.1073/pnas.1821809116, 32.
[17]
Maass C, Sorensen NB, Himmelfarb J, et al. Translational assessment of druginduced proximal tubule injury using a kidney microphysiological system. CPT Pharmacometrics Syst Pharmacol. 2019; 8 (5): 316- 325. https://doi.org/10.1002/psp4.12400.
[18]
Qu Y, An F, Luo Y, et al. A nephron model for study of drug-induced acute kidney injury and assessment of drug-induced nephrotoxicity. Biomaterials. 2018; 155: 41- 53. https://doi.org/10.1016/j.biomaterials.2017.11.010.
[19]
Xie R, Korolj A, Liu C, et al. H-fiber: microfluidic topographical hollow fiber for studies of glomerular filtration barrier. ACS Cent Sci. 2020; 6 (6): 903- 912. https://doi.org/10.1021/acscentsci.9b01097.
[20]
Petrosyan A, Cravedi P, Villani V, et al. A glomerulus-on-a-chip to recapitulate the human glomerular filtration barrier. Nat Commun. 2019;10(1):3656.https://doi.org/10.1038/s41467-019-11577-z.
[21]
Jing B, Wang ZA, Zhang C, et al. Establishment and application of peristaltic human gut-vessel microsystem for studying host-microbial interaction. Front Bioeng Biotechnol. 2020; 8: 272. https://doi.org/10.3389/fbioe.2020.00272.
[22]
Shin W, Wu A, Massidda MW, et al. A robust longitudinal co-culture of obligate anaerobic gut microbiome with human intestinal epithelium in an anoxic-oxic interface-on-a-chip. Front Bioeng Biotechnol. 2019;7(13).https://doi.org/10.3389/fbioe.2019.00013.
[23]
Bein A, Shin W, Jalili-Firoozinezhad S, et al. Microfluidic organ-on-a-chip models of human intestine. Cell Mol Gastroenterol Hepatol. 2018; 5 (4): 659- 668. https://doi.org/10.1016/j.jcmgh.2017.12.010.
[24]
Sakata T. Pitfalls in short-chain fatty acid research: a methodological review. Anim Sci J. 2019; 90 (1): 3- 13. https://doi.org/10.1111/asj.13118.
[25]
Bein A, Kim S, Goyal G, et al. Enteric coronavirus infection and treatment modeled with an immunocompetent human intestine-on-a-chip. Front Pharmacol. 2021;12,718484.https://doi.org/10.3389/fphar.2021.718484.
[26]
Nelson MT, Charbonneau MR, Coia HG, et al. Characterization of an engineered live bacterial therapeutic for the treatment of phenylketonuria in a human gut-on-achip. Nat Commun. 2021;12(1):2805.https://doi.org/10.1038/s41467-021-23072-5.
[27]
Pocock K, Delon LC, Khatri A, et al. Uptake of silica particulate drug carriers in an intestine-on-a-chip: towards a better in vitro model of nanoparticulate carrier and mucus interactions. Biomater Sci. 2019; 7 (6): 2410- 2420. https://doi.org/10.1039/c9bm00058e.
[28]
Jing B, Xia K, Zhang C, et al. Chitosan oligosaccharides regulate the occurrence and development of enteritis in a human gut-on-a-chip. Front Cell Dev Biol. 2022;10,877892.https://doi.org/10.3389/fcell.2022.877892.
[29]
Joseph X, Akhil V, Arathi A, et al. Comprehensive development in organ-on-a-chip technology. J Pharmaceut Sci. 2022; 111 (1): 18- 31. https://doi.org/10.1016/j.xphs.2021.07.014.
[30]
Tang Y, Tian F, Miao X, et al. Heart-on-a-chip using human ipsc-derived cardiomyocytes with an integrated vascular endothelial layer based on a culture patch as a potential platform for drug evaluation. Biofabrication. 2022;15(1), 15010.https://doi.org/10.1088/1758-5090/ac975d.
[31]
Vivas A, Ijspeert C, Pan JY, et al. Generation and culture of cardiac microtissues in a microfluidic chip with a reversible open top enables electrical pacing, dynamic drug dosing and endothelial cell co-culture. Adv Mater Technol. 2022;7(7), 2101355.https://doi.org/10.1002/admt.202101355.
[32]
Ren L, Zhou X, Nasiri R, et al. Combined effects of electric stimulation and microgrooves in cardiac tissue-on-a-chip for drug screening. Small Methods. 2020; 4(10), 2000438.https://doi.org/10.1002/smtd.202000438.
[33]
Staicu CE, Jipa F, Axente E, et al. Lab-on-a-chip platforms as tools for drug screening in neuropathologies associated with blood-brain barrier alterations. Biomolecules. 2021; 11 (6): 916. https://doi.org/10.3390/biom11060916.
[34]
Maoz BM, Herland A, FitzGerald EA, et al. A linked organ-on-chip model of the human neurovascular unit reveals the metabolic coupling of endothelial and neuronal cells. Nat Biotechnol. 2018; 36 (9): 865- 874. https://doi.org/10.1038/nbt.4226.
[35]
Lee S, Chung M, Lee SR, et al. 3d brain angiogenesis model to reconstitute functional human blood-brain barrier in vitro. Biotechnol Bioeng. 2019; 117 (3): 748- 762. https://doi.org/10.1002/bit.27224.
[36]
Neto E, Monteiro AC, Leite Pereira C, et al. Micropathological chip modeling the neurovascular unit response to inflammatory bone condition. Adv Healthcare Mater. 2022;11(11), 2102305.https://doi.org/10.1002/adhm.202102305.
[37]
Park J, Wetzel I, Marriott I, et al. A 3d human triculture system modeling neurodegeneration and neuroinflammation in alzheimer’s disease. Nat Neurosci. 2018;21(7):941–951.https://doi.org/10.1038/s41593-018-0175-4.
[38]
Virlogeux A, Moutaux E, Christaller W, et al. Reconstituting corticostriatal network on-a-chip reveals the contribution of the presynaptic compartment to huntington’s disease. Cell Rep. 2018; 22 (1): 110- 122. https://doi.org/10.1016/j.celrep.2017.12.013.
[39]
Xiu Y, Xiu-Li Z, Yong L, et al. Establishment of 3d organ chip for multiplexed assessment of type 2 diabetes drugs. Prog Biochem Biophys. 2019; 46 (6): 620- 630.
[40]
Nguyen DT, van Noort D, Jeong IK, et al. Endocrine system on chip for a diabetes treatment model. Biofabrication. 2017;9(1), 15021.https://doi.org/10.1088/1758-5090/aa5cc9.
[41]
Labaki WW, Han MK. Chronic respiratory diseases: a global view. Lancet Respir Med. 2020; 8 (6): 531- 533.
[42]
Kargozar S, Seeram RA, Mozafari M. Chemistry of biomaterials: future prospects. Curr Opin Biomed Eng. 2019; 10: 181- 190. https://doi.org/10.1016/j.clinmicnews.2015.01.008.
[43]
Hiemstra PS, Tetley TD, Janes SM. Airway and alveolar epithelial cells in culture. Eur Respir J. 2019;54(5), 1900742.https://doi.org/10.1183/13993003.00742-2019.
[44]
Yang X, Li K, Zhang X, et al. Nanofiber membrane supported lung-on-a-chip microdevice for anti-cancer drug testing. Lab Chip. 2018; 18 (3): 486- 495. https://doi.org/10.1039/c7lc01224a.
[45]
Sepahvandi A, Ghaffari M, Bahmanpour AH, et al. Covid-19: insights into virus–receptor interactions. Mol Biomed. 2021;2(1):1–12.https://doi.org/10.1186/s43556-021-00033-4.
[46]
Sun AM, Hoffman T, Luu BQ, et al. Application of lung microphysiological systems to covid-19 modeling and drug discovery: a review. Bio-Design and Manufacturing. 2021;4(4):757–775.https://doi.org/10.1007/s42242-021-00136-5.
[47]
Zhang M, Wang P, Luo R, et al. Biomimetic human disease model of SARS-cov-2- induced lung injury and immune responses on organ chip system. Adv Sci. 2021; 8(3), 2002928.https://doi.org/10.1002/advs.202002928.
[48]
Hajal C, Offeddu GS, Shin Y, et al. Engineered human blood–brain barrier microfluidic model for vascular permeability analyses. Nat Protoc. 2022;17(1): 95–128.https://doi.org/10.1038/s41596-021-00635-w.
[49]
Pollet AMAO, den Toonder JMJ. Recapitulating the vasculature using organ-onchip technology. Bioengineering. 2020; 7 (1): 17. https://doi.org/10.3390/bioengineering7010017.
[50]
Zhang S, Wan Z, Kamm RD. Vascularized organoids on a chip: strategies for engineering organoids with functional vasculature. Lab Chip. 2021; 21 (3): 473- 488. https://doi.org/10.1039/d0lc01186j.
[51]
Sakurai Y, Hardy ET, Ahn B, et al. A microengineered vascularized bleeding model that integrates the principal components of hemostasis. Nat Commun. 2018;9(1):509.https://doi.org/10.1038/s41467-018-02990-x.
[52]
Osaki T, Serrano JC, Kamm RD. Cooperative effects of vascular angiogenesis and lymphangiogenesis. Regen Eng Transl Med. 2018;4(3):120–132.https://doi.org/10.1007/s40883-018-0054-2.
[53]
Koo Y, Hawkins BT, Yun Y. Three-dimensional (3d) tetra-culture brain on chip platform for organophosphate toxicity screening. Sci Rep. 2018;8(1):2841.https://doi.org/10.1038/s41598-018-20876-2.
[54]
Dhiman N, Kingshott P, Sumer H, et al. On-chip anticancer drug screening - recent progress in microfluidic platforms to address challenges in chemotherapy. Biosens Bioelectron. 2019; 137: 236- 254. https://doi.org/10.1016/j.bios.2019.02.070.
[55]
Vasan N, Baselga J, Hyman DM. A view on drug resistance in cancer. Nature. 2019; 575(7782):299–309.https://doi.org/10.1038/s41586-019-1730-1.
[56]
Shang M, Soon RH, Lim CT, et al. Microfluidic modelling of the tumor microenvironment for anti-cancer drug development. Lab Chip. 2019; 19 (3): 369- 386. https://doi.org/10.1039/c8lc00970h.
[57]
Eribol P, Uguz AK, Ulgen KO. Screening applications in drug discovery based on microfluidic technology. Biomicrofluidics. 2016;10(1), 11502.https://doi.org/10.1063/1.4940886.
[58]
Ran R, Wang HF, Hou F, et al. A microfluidic tumor-on-a-chip for assessing multifunctional liposomes' tumor targeting and anticancer efficacy. Adv Healthcare Mater. 2019;8(8), 1900015.https://doi.org/10.1002/adhm.201900015.
[59]
Chakrabarty S, Quiros-Solano WF, Kuijten MMP, et al. A microfluidic cancer-onchip platform predicts drug response using organotypic tumor slice culture. Cancer Res. 2022;82(3):510–520.https://doi.org/10.1158/0008-5472.CAN-21-0799.
[60]
Dodson KH, Echevarria FD, Li D, et al. Retina-on-a-chip: a microfluidic platform for point access signaling studies. Biomed Microdevices. 2015;17(6):1–10.https://doi.org/10.1007/s10544-015-0019-x.
[61]
Chung M, Lee S, Lee BJ, et al. Wet-amd on a chip: modeling outer blood-retinal barrier in vitro. Adv Healthcare Mater. 2018;7(2), 1700028.https://doi.org/10.1002/adhm.201700028.
[62]
Bennet D, Estlack Z, Reid T, et al. A microengineered human corneal epithelium-ona-chip for eye drops mass transport evaluation. Lab Chip. 2018; 18 (11): 1539- 1551. https://doi.org/10.1039/c8lc00158h.
[63]
Wang YI, Carmona C, Hickman JJ, et al. Multiorgan microphysiological systems for drug development: strategies, advances, and challenges. Adv Healthcare Mater. 2018;7(2), 1701000.https://doi.org/10.1002/adhm.201701000.
[64]
An F, Qu YY, Luo Y, et al. A laminated microfluidic device for comprehensive preclinical testing in the drug ADME process. Sci Rep. 2016;6, 25022.https://doi.org/10.1038/srep25022.
[65]
Liu D, Jiao S, Wei J, et al. Investigation of absorption, metabolism and toxicity of ginsenosides compound k based on human organ chips. Int J Pharm. 2020;587,119669.https://doi.org/10.1016/j.ijpharm.2020.119669.
[66]
Herland A, Maoz BM, Das D, et al. Quantitative prediction of human pharmacokinetic responses to drugs via fluidically coupled vascularized organ chips. Nat Biomed Eng. 2020;4(4):421–436.https://doi.org/10.1038/s41551-019-0498-9.
[67]
Ronaldson-Bouchard K, Teles D, Yeager K, et al. A multi-organ chip with matured tissue niches linked by vascular flow. Nat Biomed Eng. 2022;6(4):351–371.https://doi.org/10.1038/s41551-022-00882-6.
[68]
Shinha K, Nihei W, Ono T, et al. A pharmacokinetic–pharmacodynamic model based on multi-organ-on-a-chip for drug–drug interaction studies. Biomicrofluidics. 2020;14(4), 44108.https://doi.org/10.1063/5.0011545.
[69]
Rossi G, Manfrin A, Lutolf MP. Progress and potential in organoid research. Nat Rev Genet. 2018;19(11):671–687.https://doi.org/10.1038/s41576-018-0051-9.
[70]
Xie X, Li X, Song W. Tumor organoid biobank-new platform for medical research. Sci Rep. 2023;13(1):1819.https://doi.org/10.1038/s41598-023-29065-2.
[71]
Veninga V, Voest EE. Tumor organoids: opportunities and challenges to guide precision medicine. Cancer Cell. 2021; 39 (9): 1190- 1201. https://doi.org/10.1016/j.ccell.2021.07.020.
[72]
Kopper O, de Witte CJ, Lõhmussaar K, et al. An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity. Nat Med. 2019;25(5): 838–849.https://doi.org/10.1038/s41591-019-0422-6.
[73]
Wang H, Zhang C, Peng K, et al. Using patient-derived organoids to predict locally advanced or metastatic lung cancer tumor response: a real-world study. Cell Reports Medicine. 2023;4(2), 100911.https://doi.org/10.1016/j.xcrm.2022.100911.
[74]
Ding S, Hsu C, Wang Z, et al. Patient-derived micro-organospheres enable clinical precision oncology. Cell Stem Cell. 2022; 29 (6): 905- 917. https://doi.org/10.1016/j.stem.2022.04.006.
[75]
Tekguc M, Gaal RCV, Uzel SGM, et al. Kidney organoids: a pioneering model for kidney diseases. Transl Res. 2022; 250: 1- 17. https://doi.org/10.1016/j.trsl.2022.06.012.
[76]
Morizane R, Lam AQ, Freedman BS, et al. Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat Biotechnol. 2015; 33 (11): 1193- 1200. https://doi.org/10.1038/nbt.3392.
[77]
Hale LJ, Howden SE, Phipson B, et al. 3d organoid-derived human glomeruli for personalised podocyte disease modelling and drug screening. Nat Commun. 2018; 9(1):5167.https://doi.org/10.1038/s41467-018-07594-z.
[78]
Jiang S, Xu F, Jin M, et al. Development of a high-throughput micropatterned agarose scaffold for consistent and reproducible hpsc-derived liver organoids. Biofabrication. 2022;15(1), 15006.https://doi.org/10.1088/1758-5090/ac933c.
[79]
van Berlo D, Nguyen VVT, Gkouzioti V, et al. Stem cells, organoids, and organ-on-achip models for personalized in vitro drug testing. Curr Opin Toxicol. 2021; 28: 7- 14. https://doi.org/10.1016/j.cotox.2021.08.006.
[80]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126 (4): 663- 676. https://doi.org/10.1016/j.cell.2006.07.024.
[81]
Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007; 318 (5858): 1917- 1920. https://doi.org/10.1126/science.1151526.
[82]
Jang J, Yoo JE, Lee JA, et al. Disease-specific induced pluripotent stem cells: a platform for human disease modeling and drug discovery. Exp Mol Med. 2012; 44 (3): 202- 213. https://doi.org/10.3858/emm.2012.44.3.015.
[83]
Sato T, Vries RG, Snippert HJ, et al. Single lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009; 459 (7244): 262- 265. https://doi.org/10.1038/nature07935.
[84]
Barker N, Huch M, Kujala P, et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010; 6 (1): 25- 36. https://doi.org/10.1016/j.stem.2009.11.013.
[85]
Kang D, Hong G, An S, et al. Bioprinting of multiscaled hepatic lobules within a highly vascularized construct. Small. 2020;16(13), 1905505.https://doi.org/10.1002/smll.201905505.
[86]
Sun L, Yang H, Wang Y, et al. Application of a 3d bioprinted hepatocellular carcinoma cell model in antitumor drug research. Front Oncol. 2020; 10: 878. https://doi.org/10.3389/fonc.2020.00878.
[87]
Li C, Jiang Z, Yang H. Advances in 3d bioprinting technology for liver regeneration. Hepatobiliary Surg Nutr. 2022;11(6):917–919.https://doi.org/10.21037/hbsn-22-531.
[88]
Grix T, Ruppelt A, Thomas A, et al. Bioprinting perfusion-enabled liver equivalents for advanced organ-on-a-chip applications. Genes. 2018; 9 (4): 176. https://doi.org/10.3390/genes9040176.
[89]
Fransen MFJ, Addario G, Bouten CVC, et al. Bioprinting of kidney in vitro models: cells, biomaterials, and manufacturing techniques. Essays Biochem. 2021; 65 (3): 587- 602. https://doi.org/10.1042/EBC20200158.
[90]
Singh NK, Han W, Nam SA, et al. Three-dimensional cell-printing of advanced renal tubular tissue analogue. Biomaterials. 2020;232, 119734.https://doi.org/10.1016/j.biomaterials.2019.119734.
[91]
Lawlor KT, Vanslambrouck JM, Higgins JW, et al. Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation. Nat Mater. 2021; 20(2):260–271.https://doi.org/10.1038/s41563-020-00853-9.
[92]
Zhang Z, Wu C, Dai C, et al. A multi-axis robot-based bioprinting system supporting natural cell function preservation and cardiac tissue fabrication. Bioact Mater. 2022; 18: 138- 150. https://doi.org/10.1016/j.bioactmat.2022.02.009.
[93]
Li X, Deng Q, Zhuang T, et al. 3D bioprinted breast tumor model for structure–activity relationship study. Bio-des. Manuf. 2020;3:361–372.https://doi.org/10.1007/s42242-020-00085-5.
[94]
Mazzaglia C, Sheng Y, Rodrigues LN, et al. Deployable extrusion bioprinting of compartmental tumoroids with cancer associated fibroblasts for immune cell interactions. Biofabrication. 2023;15(2), 25005.https://doi.org/10.1088/1758-5090/acb1db.
[95]
Lee H, Cho DW. One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3d bioprinting technology. Lab Chip. 2016; 16 (14): 2618- 2625. https://doi.org/10.1039/c6lc00450d.
[96]
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), 25001.https://doi.org/10.1088/1758-5090/aaf9fa.
[97]
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.https://doi.org/10.1038/srep34845.
[98]
Lin NYC, Homan KA, Robinson SS, et al. Renal reabsorption in 3d vascularized proximal tubule models. Proc Natl Acad Sci USA. 2019; 116 (12): 5399- 5404. https://doi.org/10.1073/pnas.1815208116.
[99]
Park JY, Ryu H, Lee B, et al. Development of a functional airway-on-a-chip by 3d cell printing. Biofabrication. 2018;11(1), 15002.https://doi.org/10.1088/1758-5090/aae545.
[100]
Yi H, Jeong YH, Kim Y, et al. A bioprinted human-glioblastoma-on-a-chip for the identification of patient-specific responses to chemoradiotherapy. Nat Biomed Eng. 2019;3(7):509–519.https://doi.org/10.1038/s41551-019-0363-x.
[101]
Cui Y, Xiao R, Zhou Y, et al. Establishment of organoid models based on a nested array chip for fast and reproducible drug testing in colorectal cancer therapy. BioDesign and Manufacturing. 2022;5(4):674–686.https://doi.org/10.1007/s42242-022-00206-2.
[102]
Jung DJ, Shin TH, Kim M, et al. A one-stop microfluidic-based lung cancer organoid culture platform for testing drug sensitivity. Lab Chip. 2019; 19 (17): 2854- 2865. https://doi.org/10.1039/c9lc00496c.
[103]
Lee HN, Choi YY, Kim JW, et al. Effect of biochemical and biomechanical factors on vascularization of kidney organoid-on-a-chip. Nano Convergence. 2021;8(1):35.https://doi.org/10.1186/s40580-021-00285-4.
[104]
Tao T, Deng P, Wang Y, et al. Microengineered multi-organoid system from hipscs to recapitulate human liver-islet axis in normal and type 2 diabetes. Adv Sci. 2022; 9(5), 2103495.https://doi.org/10.1002/advs.202103495.
[105]
Skardal A, Aleman J, Forsythe S, et al. Drug compound screening in single and integrated multi-organoid body-on-a-chip systems. Biofabrication. 2020;12(2),25017.https://doi.org/10.1088/1758-5090/ab6d36.

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