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Current Stem Cell Research & Therapy

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ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

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Review Article

Co-culture of Liver Parenchymal Cells with Non-parenchymal Cells Under 2D and 3D Culture Systems; A Review

Author(s): Zahra Farzaneh, Fatemeh Khojastehpour, Mona Keivan and Maryam Farzaneh*

Volume 18, Issue 7, 2023

Published on: 16 September, 2022

Page: [904 - 916] Pages: 13

DOI: 10.2174/1574888X17666220614160957

Price: $65

Abstract

Hepatocytes are the major parenchymal cells (PC) in the liver and present an important role in liver metabolism. Hepatocytes are considered a gold standard tool for drug toxicity/screening or liver disease modeling. However, the maturation and functions of hepatocytes are lost under routine 2- dimensional (2D) culture conditions. Recent studies revealed that the interactions between hepatocytes and non-parenchyma cells (NPC) under 3D culture conditions can be an alternative option for optimizing hepatocyte maturation. Co-culture of hepatocytes with NPC simplifies the in-vitro liver disease models of fibrosis, steatosis and non-alcoholic fatty liver disease (NAFLD), cholestasis, and viral hepatitis. This review described the co-culture of liver PC with NPC under 2D and 3D culture systems.

Keywords: Liver disease, hepatocytes, non-parenchyma cells, co-culture, steatosis, metabolism.

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[1]
Asrani SK, Devarbhavi H, Eaton J, Kamath PS. Burden of liver diseases in the world. J Hepatol 2019; 70(1): 151-71.
[http://dx.doi.org/10.1016/j.jhep.2018.09.014] [PMID: 30266282]
[2]
Ahmad MS, Suardi N, Shukri A, et al. Chemical characteristics, motivation and strategies in choice of materials used as liver phantom: A literature review. J Med Ultrasound 2020; 28(1): 7-16.
[PMID: 32368444]
[3]
Nevzorova YA, Boyer-Diaz Z, Cubero FJ, Gracia-Sancho J. Animal models for liver disease - A practical approach for translational research. J Hepatol 2020; 73(2): 423-40.
[http://dx.doi.org/10.1016/j.jhep.2020.04.011] [PMID: 32330604]
[4]
Shin HK, Kang MG, Park D, Park T, Yoon S. Development of prediction models for drug-induced cholestasis, cirrhosis, hepatitis, and steatosis based on drug and drug metabolite structures. Front Pharmacol 2020; 11: 67.
[http://dx.doi.org/10.3389/fphar.2020.00067] [PMID: 32116729]
[5]
Collins SD, Yuen G, Tu T. et al. In vitro models of the liver: Disease modeling, drug discovery and clinical applications. In: Tirnitz-Parker JEE, Ed. Hepatocellular Carcinoma. Brisbane (AU) 2019.
[6]
Jin M, Yi X, Liao W, et al. Advancements in stem cell-derived hepatocyte-like cell models for hepatotoxicity testing. Stem Cell Res Ther 2021; 12(1): 84.
[http://dx.doi.org/10.1186/s13287-021-02152-9] [PMID: 33494782]
[7]
Zhang H, Shao X, Zhao H, et al. Integration of metabolomics and lipidomics reveals metabolic mechanisms of triclosan-induced toxicity in human hepatocytes. Environ Sci Technol 2019; 53(9): 5406-15.
[http://dx.doi.org/10.1021/acs.est.8b07281] [PMID: 30964272]
[8]
Almazroo OA, Miah MK, Venkataramanan R. Drug metabolism in the liver. Clin Liver Dis 2017; 21(1): 1-20.
[http://dx.doi.org/10.1016/j.cld.2016.08.001] [PMID: 27842765]
[9]
Tsuchiya A, Lu W-Y. Liver stem cells: Plasticity of the liver epithelium. World J Gastroenterol 2019; 25(9): 1037-49.
[http://dx.doi.org/10.3748/wjg.v25.i9.1037] [PMID: 30862993]
[10]
Forouzesh M, Hosseini M, Ataei M, Farzaneh M, Khoshnam SE. An extracellular matrix-based culture system for generation of human pluripotent stem cell derived-hepatocytes. Curr Stem Cell Res Ther 2020; 16(7): 888-96.
[PMID: 33371861]
[11]
Raven A, Lu W-Y, Man TY, et al. Cholangiocytes act as facultative liver stem cells during impaired hepatocyte regeneration. Nature 2017; 547(7663): 350-4.
[http://dx.doi.org/10.1038/nature23015] [PMID: 28700576]
[12]
Matsumoto T, Wakefield L, Tarlow BD, Grompe M. In vivo lineage tracing of polyploid hepatocytes reveals extensive proliferation during liver regeneration. Cell Stem Cell 2020; 26: 34-47.
[http://dx.doi.org/10.1016/j.stem.2019.11.014]
[13]
Katoonizadeh A, Poustchi H, Malekzadeh R. Hepatic progenitor cells in liver regeneration: Current advances and clinical perspectives. Liver Int 2014; 34(10): 1464-72.
[http://dx.doi.org/10.1111/liv.12573] [PMID: 24750779]
[14]
Zeilinger K, Freyer N, Damm G, Seehofer D, Knöspel F. Cell sources for in vitro human liver cell culture models. Exp Biol Med (Maywood) 2016; 241(15): 1684-98.
[http://dx.doi.org/10.1177/1535370216657448] [PMID: 27385595]
[15]
Hendriks DF, Fredriksson Puigvert L, Messner S, Mortiz W, Ingelman-Sundberg M. Hepatic 3D spheroid models for the detection and study of compounds with cholestatic liability. Sci Rep 2016; 6: 35434.
[http://dx.doi.org/10.1038/srep35434] [PMID: 27759057]
[16]
Yao T, Zhang Y, Lv M, Zang G, Ng SS, Chen X. Three-dimensional cell culture model for hepatocytes opens a new avenue of real world research on liver arXiv preprint arXiv.191108231 2019.
[17]
Milner E, Ainsworth M, McDonough M, et al. Emerging three-dimensional hepatic models in relation to traditional two-dimensional in vitro assays for evaluating drug metabolism and hepatoxicity. Medicine in Drug Discovery 2020; 8: 100060.
[http://dx.doi.org/10.1016/j.medidd.2020.100060]
[18]
Sato K, Kennedy L, Liangpunsakul S, et al. Intercellular Communication between Hepatic Cells in Liver Diseases. Int J Mol Sci 2019; 20(9): 20.
[http://dx.doi.org/10.3390/ijms20092180] [PMID: 31052525]
[19]
Kostadinova R, Boess F, Applegate D, et al. A long-term three dimensional liver co-culture system for improved prediction of clinically relevant drug-induced hepatotoxicity. Toxicol Appl Pharmacol 2013; 268(1): 1-16.
[http://dx.doi.org/10.1016/j.taap.2013.01.012] [PMID: 23352505]
[20]
Bell CC, Hendriks DF, Moro SM, et al. Characterization of primary human hepatocyte spheroids as a model system for drug-induced liver injury, liver function and disease. Sci Rep 2016; 6: 25187.
[http://dx.doi.org/10.1038/srep25187] [PMID: 27143246]
[21]
Krishna M. Microscopic anatomy of the liver. Clin Liver Dis (Hoboken) 2013; 2 (Suppl. 1): S4-7.
[http://dx.doi.org/10.1002/cld.147] [PMID: 30992875]
[22]
Ugo L, Brocco S, Merola A, Mescoli C, Quaia E. Liver Anatomy Imaging of the Liver and Intra-hepatic Biliary Tract. Springer 2020; pp. 15-47.
[23]
Kholodenko IV, Yarygin KN. Cellular Mechanisms of Liver Regeneration and Cell-Based Therapies of Liver Diseases. BioMed Res Int 2017; 2017: 8910821-1.
[http://dx.doi.org/10.1155/2017/8910821] [PMID: 28210629]
[24]
Boyer JL. Bile formation and secretion. Compr Physiol 2013; 3(3): 1035-78.
[http://dx.doi.org/10.1002/cphy.c120027] [PMID: 23897680]
[25]
Schulze RJ, Schott MB, Casey CA, Tuma PL, McNiven MA. The cell biology of the hepatocyte: A membrane trafficking machine. J Cell Biol 2019; 218(7): 2096-112.
[http://dx.doi.org/10.1083/jcb.201903090] [PMID: 31201265]
[26]
Stanger BZ. Cellular homeostasis and repair in the mammalian liver. Annu Rev Physiol 2015; 77: 179-200.
[http://dx.doi.org/10.1146/annurev-physiol-021113-170255] [PMID: 25668020]
[27]
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 (Basel) 2019; 10(10): 10.
[http://dx.doi.org/10.3390/mi10100676] [PMID: 31591365]
[28]
Sanz-García C, Fernández-Iglesias A, Gracia-Sancho J, Arráez-Aybar LA, Nevzorova YA, Cubero FJ. The space of disse: The liver hub in health and disease. Livers 2021; 1: 3-26.
[http://dx.doi.org/10.3390/livers1010002]
[29]
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.
[http://dx.doi.org/10.1080/15476278.2016.1278133] [PMID: 28055309]
[30]
Abu Rmilah A, Zhou W, Nelson E, Lin L, Amiot B, Nyberg SL. Understanding the marvels behind liver regeneration. Wiley Interdiscip Rev Dev Biol 2019; 8(3): e340.
[http://dx.doi.org/10.1002/wdev.340] [PMID: 30924280]
[31]
Arriazu E, Ruiz de Galarreta M, Cubero FJ, et al. Extracellular matrix and liver disease. Antioxid Redox Signal 2014; 21(7): 1078-97.
[http://dx.doi.org/10.1089/ars.2013.5697] [PMID: 24219114]
[32]
McQuitty CE, Williams R, Chokshi S, Urbani L. Immunomodulatory role of the extracellular matrix within the liver disease microenvironment. Front Immunol 2020; 11: 574276-6.
[http://dx.doi.org/10.3389/fimmu.2020.574276] [PMID: 33262757]
[33]
Martinez-Hernandez A, Amenta PS. The hepatic extracellular matrix. II. Ontogenesis, regeneration and cirrhosis. Virchows Arch A Pathol Anat Histopathol 1993; 423(2): 77-84.
[http://dx.doi.org/10.1007/BF01606580] [PMID: 8212543]
[34]
Klaas M, Kangur T, Viil J, et al. The alterations in the extracellular matrix composition guide the repair of damaged liver tissue. Sci Rep 2016; 6: 27398.
[http://dx.doi.org/10.1038/srep27398] [PMID: 27264108]
[35]
LeCluyse EL, Witek RP, Andersen ME, Powers MJ. Organotypic liver culture models: Meeting current challenges in toxicity testing. Crit Rev Toxicol 2012; 42(6): 501-48.
[http://dx.doi.org/10.3109/10408444.2012.682115] [PMID: 22582993]
[36]
Otsuka H, Sasaki K, Okimura S, Nagamura M, Nakasone Y. Micropatterned co-culture of hepatocyte spheroids layered on non-parenchymal cells to understand heterotypic cellular interactions. Sci Technol Adv Mater 2013; 14(6): 065003.
[http://dx.doi.org/10.1088/1468-6996/14/6/065003] [PMID: 27877623]
[37]
Wang G, Zheng Y, Wang Y, et al. Co-culture system of hepatocytes and endothelial cells: Two in vitro approaches for enhancing liver-specific functions of hepatocytes. Cytotechnology 2018; 70(4): 1279-90.
[http://dx.doi.org/10.1007/s10616-018-0219-3] [PMID: 29675734]
[38]
Cho CH, Park J, Tilles AW, Berthiaume F, Toner M, Yarmush ML. Layered patterning of hepatocytes in co-culture systems using microfabricated stencils. Biotechniques 2010; 48(1): 47-52.
[http://dx.doi.org/10.2144/000113317] [PMID: 20078427]
[39]
Ware BR, Durham MJ, Monckton CP, Khetani SR. A cell culture platform to maintain long-term phenotype of primary human hepatocytes and endothelial cells. Cell Mol Gastroenterol Hepatol 2017; 5(3): 187-207.
[http://dx.doi.org/10.1016/j.jcmgh.2017.11.007] [PMID: 29379855]
[40]
Khetani SR, Bhatia SN. Microscale culture of human liver cells for drug development. Nat Biotechnol 2008; 26(1): 120-6.
[http://dx.doi.org/10.1038/nbt1361] [PMID: 18026090]
[41]
Kim K, Ohashi K, Utoh R, Kano K, Okano T. Preserved liver-specific functions of hepatocytes in 3D co-culture with endothelial cell sheets. Biomaterials 2012; 33(5): 1406-13.
[http://dx.doi.org/10.1016/j.biomaterials.2011.10.084] [PMID: 22118777]
[42]
Hirose M, Yamato M, Kwon OH, et al. Temperature-Responsive surface for novel co-culture systems of hepatocytes with endothelial cells: 2-D patterned and double layered co-cultures. Yonsei Med J 2000; 41(6): 803-13.
[http://dx.doi.org/10.3349/ymj.2000.41.6.803] [PMID: 11204831]
[43]
Kasuya J, Sudo R, Mitaka T, Ikeda M, Tanishita K. Spatio-temporal control of hepatic stellate cell-endothelial cell interactions for reconstruction of liver sinusoids in vitro. Tissue Eng Part A 2012; 18(9-10): 1045-56.
[http://dx.doi.org/10.1089/ten.tea.2011.0351] [PMID: 22220631]
[44]
Bale SS, Geerts S, Jindal R, Yarmush ML. Isolation and co-culture of rat parenchymal and non-parenchymal liver cells to evaluate cellular interactions and response. Sci Rep 2016; 6: 25329.
[http://dx.doi.org/10.1038/srep25329] [PMID: 27142224]
[45]
Choi YY, Seok JI, Kim DS. Flow-based three-dimensional co-culture model for long-term hepatotoxicity prediction. Micromachines (Basel) 2019; 11(1): 11.
[http://dx.doi.org/10.3390/mi11010036] [PMID: 31892214]
[46]
Lee S-A, No Y, Kang E, Ju J, Kim DS, Lee SH. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab Chip 2013; 13(18): 3529-37.
[http://dx.doi.org/10.1039/c3lc50197c] [PMID: 23657720]
[47]
Zhou Y, Shen JX, Lauschke VM. Comprehensive evaluation of organotypic and microphysiological liver models for prediction of drug-induced liver injury. Front Pharmacol 2019; 10: 1093.
[http://dx.doi.org/10.3389/fphar.2019.01093] [PMID: 31616302]
[48]
Yagi K, Tsuda K, Serada M, Yamada C, Kondoh A, Miura Y. Rapid formation of multicellular spheroids of adult rat hepatocytes by rotation culture and their immobilization within calcium alginate. Artif Organs 1993; 17(11): 929-34.
[http://dx.doi.org/10.1111/j.1525-1594.1993.tb00405.x] [PMID: 7906511]
[49]
Richert L, Baze A, Parmentier C, et al. Cytotoxicity evaluation using cryopreserved primary human hepatocytes in various culture formats. Toxicol Lett 2016; 258: 207-15.
[http://dx.doi.org/10.1016/j.toxlet.2016.06.1127] [PMID: 27363785]
[50]
Messner S, Agarkova I, Moritz W, Kelm JM. Multi-cell type human liver microtissues for hepatotoxicity testing. Arch Toxicol 2013; 87(1): 209-13.
[http://dx.doi.org/10.1007/s00204-012-0968-2] [PMID: 23143619]
[51]
Chen Q, Utech S, Chen D, Prodanovic R, Lin JM, Weitz DA. Controlled assembly of heterotypic cells in a core-shell scaffold: Organ in a droplet. Lab Chip 2016; 16(8): 1346-9.
[http://dx.doi.org/10.1039/C6LC00231E] [PMID: 26999495]
[52]
Kukla DA, Crampton AL, Wood DK, Khetani SR. Microscale collagen and fibroblast interactions enhance primary human hepatocyte functions in three-dimensional models. Gene Expr 2020; 20(1): 1-18.
[http://dx.doi.org/10.3727/105221620X15868728381608] [PMID: 32290899]
[53]
Novik E, Maguire TJ, Chao P, Cheng KC, Yarmush ML. A microfluidic hepatic coculture platform for cell-based drug metabolism studies. Biochem Pharmacol 2010; 79(7): 1036-44.
[http://dx.doi.org/10.1016/j.bcp.2009.11.010] [PMID: 19925779]
[54]
Vernetti LA, Senutovitch N, Boltz R, et al. A human liver microphysiology platform for investigating physiology, drug safety, and disease models. Exp Biol Med (Maywood) 2016; 241(1): 101-14.
[http://dx.doi.org/10.1177/1535370215592121] [PMID: 26202373]
[55]
Zhou Y, Shen JX, Lauschke VM. Comprehensive evaluation of current organotypic and microphysiological liver models for prediction of drug-induced liver injury. Front Pharmacol 2019; 10: 1093.
[http://dx.doi.org/10.3389/fphar.2019.01093] [PMID: 31616302]
[56]
Barrero JJ, Pagazartaundua A, Glick BS, Valero F, Ferrer P. Bioreactor-scale cell performance and protein production can be substantially increased by using a secretion signal that drives co-translational translocation in Pichia pastoris. N Biotechnol 2021; 60: 85-95.
[http://dx.doi.org/10.1016/j.nbt.2020.09.001] [PMID: 33045421]
[57]
Salerno S, Tasselli F, Drioli E, De Bartolo L. Poly(ε-Caprolactone) hollow fiber membranes for the biofabrication of a vascularized human liver tissue. Membranes (Basel) 2020; 10(6): 112.
[http://dx.doi.org/10.3390/membranes10060112] [PMID: 32471264]
[58]
Okudaira T, Yabuta R, Mizumoto H, Kajiwara T. Fabrication of a fiber-type hepatic tissue by bottom-up method using multilayer spheroids. J Biosci Bioeng 2017; 123(6): 739-47.
[http://dx.doi.org/10.1016/j.jbiosc.2017.01.002] [PMID: 28131540]
[59]
Rebelo SP, Costa R, Silva MM, Marcelino P, Brito C, Alves PM. Three-dimensional co-culture of human hepatocytes and mesenchymal stem cells: Improved functionality in long-term bioreactor cultures. J Tissue Eng Regen Med 2017; 11(7): 2034-45.
[http://dx.doi.org/10.1002/term.2099] [PMID: 26511086]
[60]
Zhao X, Zhu Y, Laslett AL, Chan HF. Hepatic Differentiation of Stem Cells in 2D and 3D Biomaterial Systems. Bioengineering (Basel) 2020; 7(2): 7.
[http://dx.doi.org/10.3390/bioengineering7020047] [PMID: 32466173]
[61]
Shakado S, Sakisaka S, Noguchi K, et al. Effects of extracellular matrices on tube formation of cultured rat hepatic sinusoidal endothelial cells. Hepatology 1995; 22(3): 969-73.
[http://dx.doi.org/10.1002/hep.1840220339] [PMID: 7657305]
[62]
Chen AX, Chhabra A, Fleming HE, Bhatia SN. Hepatic tissue engineering Principles of Tissue Engineering. (5th ed.). Academic Press 2020; pp. 737-53.
[http://dx.doi.org/10.1016/B978-0-12-818422-6.00041-1]
[63]
Wei G, Wang J, Lv Q, et al. Three-dimensional coculture of primary hepatocytes and stellate cells in silk scaffold improves hepatic morphology and functionality in vitro. J Biomed Mater Res A 2018; 106(8): 2171-80.
[http://dx.doi.org/10.1002/jbm.a.36421] [PMID: 29607608]
[64]
Du C, Narayanan K, Leong MF, Wan AC. Induced pluripotent stem cell-derived hepatocytes and endothelial cells in multi-component hydrogel fibers for liver tissue engineering. Biomaterials 2014; 35(23): 6006-14.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.011] [PMID: 24780169]
[65]
Freyer N, Greuel S, Knöspel F, et al. Effects of co-culture media on hepatic differentiation of hiPSC with or without HUVEC co-culture. Int J Mol Sci 2017; 18(8): 18.
[http://dx.doi.org/10.3390/ijms18081724] [PMID: 28783133]
[66]
Li F, Cao L, Parikh S, Zuo R. Three-dimensional spheroids with primary human liver cells and differential roles of kupffer cells in drug-induced liver injury. J Pharm Sci 2020; 109(6): 1912-23.
[http://dx.doi.org/10.1016/j.xphs.2020.02.021] [PMID: 32145211]
[67]
Davidson MD, Khetani SR. Intermittent starvation extends the functional lifetime of primary human hepatocyte cultures. Toxicol Sci 2020; 174(2): 266-77.
[http://dx.doi.org/10.1093/toxsci/kfaa003] [PMID: 31977024]
[68]
Qin HH, Filippi C, Sun S, Lehec S, Dhawan A, Hughes RD. Hypoxic preconditioning potentiates the trophic effects of mesenchymal stem cells on co-cultured human primary hepatocytes. Stem Cell Res Ther 2015; 6: 237.
[http://dx.doi.org/10.1186/s13287-015-0218-7] [PMID: 26626568]
[69]
Glicklis R, Merchuk JC, Cohen S. Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol Bioeng 2004; 86(6): 672-80.
[http://dx.doi.org/10.1002/bit.20086] [PMID: 15137079]
[70]
Hurrell T, Kastrinou-Lampou V, Fardellas A, et al. Human liver spheroids as a model to study aetiology and treatment of hepatic fibrosis. Cells 2020; 9(4): 9.
[http://dx.doi.org/10.3390/cells9040964] [PMID: 32295224]
[71]
Chen F, Wang H, Xiao J. Regulated differentiation of stem cells into an artificial 3D liver as a transplantable source. Clin Mol Hepatol 2020; 26(2): 163-79.
[http://dx.doi.org/10.3350/cmh.2019.0022n] [PMID: 32098013]
[72]
Poisson J, Lemoinne S, Boulanger C, et al. Liver sinusoidal endothelial cells: Physiology and role in liver diseases. J Hepatol 2017; 66(1): 212-27.
[http://dx.doi.org/10.1016/j.jhep.2016.07.009] [PMID: 27423426]
[73]
Zhang XJ, Olsavszky V, Yin Y, et al. Angiocrine hepatocyte growth factor signaling controls physiological organ and body size and dynamic hepatocyte proliferation to prevent liver damage during regeneration. Am J Pathol 2020; 190(2): 358-71.
[http://dx.doi.org/10.1016/j.ajpath.2019.10.009] [PMID: 31783007]
[74]
Shetty S, Lalor PF, Adams DH. Liver sinusoidal endothelial cells - gatekeepers of hepatic immunity. Nat Rev Gastroenterol Hepatol 2018; 15(9): 555-67.
[http://dx.doi.org/10.1038/s41575-018-0020-y] [PMID: 29844586]
[75]
Kidambi S, Yarmush RS, Novik E, Chao P, Yarmush ML, Nahmias Y. Oxygen-mediated enhancement of primary hepatocyte metabolism, functional polarization, gene expression, and drug clearance. Proc Natl Acad Sci USA 2009; 106(37): 15714-9.
[http://dx.doi.org/10.1073/pnas.0906820106] [PMID: 19720996]
[76]
Lalor PF, Lai WK, Curbishley SM, Shetty S, Adams DH. Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions in vivo. World J Gastroenterol 2006; 12(34): 5429-39.
[http://dx.doi.org/10.3748/wjg.v12.i34.5429] [PMID: 17006978]
[77]
Kim Y, Rajagopalan P. 3D hepatic cultures simultaneously maintain primary hepatocyte and liver sinusoidal endothelial cell phenotypes. PLoS One 2010; 5(11): e15456.
[http://dx.doi.org/10.1371/journal.pone.0015456] [PMID: 21103392]
[78]
Xiong A, Austin TW, Lagasse E, et al. Isolation of human fetal liver progenitors and their enhanced proliferation by three-dimensional coculture with endothelial cells. Tissue Eng Part A 2008; 14(6): 995-1006.
[http://dx.doi.org/10.1089/ten.tea.2007.0087] [PMID: 19230124]
[79]
Bale SS, Golberg I, Jindal R, et al. Long-term coculture strategies for primary hepatocytes and liver sinusoidal endothelial cells. Tissue Eng Part C Methods 2015; 21(4): 413-22.
[http://dx.doi.org/10.1089/ten.tec.2014.0152] [PMID: 25233394]
[80]
Kunkanjanawan H, Kunkanjanawan T, Khemarangsan V, Yodsheewan R, Theerakittayakorn K, Parnpai R. A xeno-free strategy for derivation of human umbilical vein endothelial cells and wharton’s jelly derived mesenchymal stromal cells: A feasibility study toward personal cell and vascular based therapy Stem Cells International. 2020; 2020
[http://dx.doi.org/10.1155/2020/8832052 ]
[81]
Kocherova I, Bryja A, Mozdziak P, et al. Human umbilical vein endothelial cells (HUVECs) co-culture with osteogenic cells: From molecular communication to engineering prevascularised bone grafts. J Clin Med 2019; 8(10): 8.
[http://dx.doi.org/10.3390/jcm8101602] [PMID: 31623330]
[82]
Guo X, Li W, Ma M, Lu X, Zhang H. Endothelial cell-derived matrix promotes the metabolic functional maturation of hepatocyte via integrin-Src signalling. J Cell Mol Med 2017; 21(11): 2809-22.
[http://dx.doi.org/10.1111/jcmm.13195] [PMID: 28470937]
[83]
Lua I, Asahina K. The role of mesothelial cells in liver development, injury, and regeneration. Gut Liver 2016; 10(2): 166-76.
[http://dx.doi.org/10.5009/gnl15226] [PMID: 26934883]
[84]
Ahmed HMM, Salerno S, Morelli S, Giorno L, De Bartolo L. 3D liver membrane system by co-culturing human hepatocytes, sinusoidal endothelial and stellate cells. Biofabrication 2017; 9(2): 025022.
[http://dx.doi.org/10.1088/1758-5090/aa70c7] [PMID: 28548045]
[85]
Weiskirchen R, Tacke F. Cellular and molecular functions of hepatic stellate cells in inflammatory responses and liver immunology. Hepatobiliary Surg Nutr 2014; 3(6): 344-63.
[PMID: 25568859]
[86]
Feaver RE, Cole BK, Lawson MJ, et al. Development of an in vitro human liver system for interrogating nonalcoholic steatohepatitis. JCI Insight 2016; 1(20): e90954.
[http://dx.doi.org/10.1172/jci.insight.90954] [PMID: 27942596]
[87]
Barbero-Becerra VJ, Giraudi PJ, Chávez-Tapia NC, Uribe M, Tiribelli C, Rosso N. The interplay between hepatic stellate cells and hepatocytes in an in vitro model of NASH. Toxicol In Vitro 2015; 29(7): 1753-8.
[http://dx.doi.org/10.1016/j.tiv.2015.07.010] [PMID: 26187275]
[88]
Coll M, Perea L, Boon R, et al. Generation of hepatic stellate cells from human pluripotent stem cells enables in vitro modeling of liver fibrosis. Cell Stem Cell 2018; 23(1): 101-113.e7.
[http://dx.doi.org/10.1016/j.stem.2018.05.027] [PMID: 30049452]
[89]
Wong SF, No Y, Choi YY, Kim DS, Chung BG, Lee SH. Concave microwell based size-controllable hepatosphere as a three-dimensional liver tissue model. Biomaterials 2011; 32(32): 8087-96.
[http://dx.doi.org/10.1016/j.biomaterials.2011.07.028] [PMID: 21813175]
[90]
Thomas RJ, Bhandari R, Barrett DA, et al. The effect of three-dimensional co-culture of hepatocytes and hepatic stellate cells on key hepatocyte functions in vitro. Cells Tissues Organs 2005; 181(2): 67-79.
[http://dx.doi.org/10.1159/000091096] [PMID: 16534201]
[91]
Leite SB, Roosens T, El Taghdouini A, et al. Novel human hepatic organoid model enables testing of drug-induced liver fibrosis in vitro. Biomaterials 2016; 78: 1-10.
[http://dx.doi.org/10.1016/j.biomaterials.2015.11.026] [PMID: 26618472]
[92]
Zhou VX, Lolas M, Chang TT. Direct orthotopic implantation of hepatic organoids. J Surg Res 2017; 211: 251-60.
[http://dx.doi.org/10.1016/j.jss.2016.12.028] [PMID: 28501125]
[93]
Davidson MD, Kukla DA, Khetani SR. Microengineered cultures containing human hepatic stellate cells and hepatocytes for drug development. Integr Biol 2017; 9(8): 662-77.
[http://dx.doi.org/10.1039/C7IB00027H] [PMID: 28702667]
[94]
Prestigiacomo V, Weston A, Messner S, Lampart F, Suter-Dick L. Pro-fibrotic compounds induce stellate cell activation, ECM-remodelling and Nrf2 activation in a human 3D-multicellular model of liver fibrosis. PLoS One 2017; 12(6): e0179995.
[http://dx.doi.org/10.1371/journal.pone.0179995] [PMID: 28665955]
[95]
Wirz W, Antoine M, Tag CG, et al. Hepatic stellate cells display a functional vascular smooth muscle cell phenotype in a three-dimensional co-culture model with endothelial cells. Differentiation 2008; 76(7): 784-94.
[http://dx.doi.org/10.1111/j.1432-0436.2007.00260.x] [PMID: 18177423]
[96]
Nguyen TV, Ukairo O, Khetani SR, et al. Establishment of a hepatocyte-kupffer cell coculture model for assessment of proinflammatory cytokine effects on metabolizing enzymes and drug transporters. Drug Metab Dispos 2015; 43(5): 774-85.
[http://dx.doi.org/10.1124/dmd.114.061317] [PMID: 25739975]
[97]
Rose KA, Holman NS, Green AM, Andersen ME, LeCluyse EL. Co-culture of hepatocytes and kupffer cells as an in vitro model of inflammation and drug-induced hepatotoxicity. J Pharm Sci 2016; 105(2): 950-64.
[http://dx.doi.org/10.1016/S0022-3549(15)00192-6] [PMID: 26869439]
[98]
Granitzny A, Knebel J, Müller M, et al. Evaluation of a human in vitro hepatocyte-NPC co-culture model for the prediction of idiosyncratic drug-induced liver injury: A pilot study. Toxicol Rep 2017; 4: 89-103.
[http://dx.doi.org/10.1016/j.toxrep.2017.02.001] [PMID: 28959630]
[99]
Ware BR, Berger DR, Khetani SR. Prediction of drug-induced liver injury in micropatterned co-cultures containing iPSC-derived human hepatocytes. Toxicol Sci 2015; 145(2): 252-62.
[http://dx.doi.org/10.1093/toxsci/kfv048] [PMID: 25716675]
[100]
Novik EI, Dwyer J, Morelli JK, et al. Long-enduring primary hepatocyte-based co-cultures improve prediction of hepatotoxicity. Toxicol Appl Pharmacol 2017; 336: 20-30.
[http://dx.doi.org/10.1016/j.taap.2017.09.013] [PMID: 28942002]
[101]
Liu Y, Li H, Yan S, Wei J, Li X. Hepatocyte cocultures with endothelial cells and fibroblasts on micropatterned fibrous mats to promote liver-specific functions and capillary formation capabilities. Biomacromolecules 2014; 15(3): 1044-54.
[http://dx.doi.org/10.1021/bm401926k] [PMID: 24547870]
[102]
Gu J, Shi X, Zhang Y, Ding Y. Heterotypic interactions in the preservation of morphology and functionality of porcine hepatocytes by bone marrow mesenchymal stem cells in vitro. J Cell Physiol 2009; 219(1): 100-8.
[http://dx.doi.org/10.1002/jcp.21651] [PMID: 19086033]
[103]
Chen QH, Liu AR, Qiu HB, Yang Y. Interaction between mesenchymal stem cells and endothelial cells restores endothelial permeability via paracrine hepatocyte growth factor in vitro. Stem Cell Res Ther 2015; 6: 44.
[http://dx.doi.org/10.1186/s13287-015-0025-1] [PMID: 25888925]
[104]
Meier F, Freyer N, Brzeszczynska J, et al. Hepatic differentiation of human iPSCs in different 3D models: A comparative study. Int J Mol Med 2017; 40(6): 1759-71.
[http://dx.doi.org/10.3892/ijmm.2017.3190] [PMID: 29039463]
[105]
Peng WC, Kraaier LJ, Kluiver TA. Hepatocyte organoids and cell transplantation: What the future holds. Exp Mol Med 2021; 53(10): 1512-28.
[http://dx.doi.org/10.1038/s12276-021-00579-x] [PMID: 34663941]
[106]
Jensen C, Teng Y. Is it time to start transitioning from 2D to 3D cell culture? Front Mol Biosci 2020; 7: 33.
[http://dx.doi.org/10.3389/fmolb.2020.00033] [PMID: 32211418]
[107]
Fernandez-Checa JC, Bagnaninchi P, Ye H, et al. Advanced preclinical models for evaluation of drug-induced liver injury - consensus statement by the European Drug-Induced Liver Injury Network.[PRO-EURO-DILI-NET]. J Hepatol 2021; 75(4): 935-59.
[http://dx.doi.org/10.1016/j.jhep.2021.06.021] [PMID: 34171436]
[108]
March S, Ng S, Velmurugan S, et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe 2013; 14(1): 104-15.
[http://dx.doi.org/10.1016/j.chom.2013.06.005] [PMID: 23870318]
[109]
Fukuda J, Khademhosseini A, Yeh J, et al. Micropatterned cell co-cultures using layer-by-layer deposition of extracellular matrix components. Biomaterials 2006; 27(8): 1479-86.
[http://dx.doi.org/10.1016/j.biomaterials.2005.09.015] [PMID: 16242769]
[110]
Fitzpatrick E, Wu Y, Dhadda P, et al. Coculture with mesenchymal stem cells results in improved viability and function of human hepatocytes. Cell Transplant 2015; 24(1): 73-83.
[http://dx.doi.org/10.3727/096368913X674080] [PMID: 24143888]
[111]
Zinchenko YS, Schrum LW, Clemens M, Coger RN. Hepatocyte and kupffer cells co-cultured on micropatterned surfaces to optimize hepatocyte function. Tissue Eng 2006; 12(4): 751-61.
[http://dx.doi.org/10.1089/ten.2006.12.751] [PMID: 16674289]
[112]
Michalopoulos GK, Bowen WC, Mulè K, Stolz DB. Histological organization in hepatocyte organoid cultures. Am J Pathol 2001; 159(5): 1877-87.
[http://dx.doi.org/10.1016/S0002-9440(10)63034-9] [PMID: 11696448]
[113]
Wang WW, Khetani SR, Krzyzewski S, Duignan DB, Obach RS. Assessment of a micropatterned hepatocyte coculture system to generate major human excretory and circulating drug metabolites. Drug Metab Dispos 2010; 38(10): 1900-5.
[http://dx.doi.org/10.1124/dmd.110.034876] [PMID: 20595376]
[114]
Baze A, Parmentier C, Hendriks DFG, et al. Three-dimensional spheroid primary human hepatocytes in monoculture and coculture with nonparenchymal cells. Tissue Eng Part C Methods 2018; 24(9): 534-45.
[http://dx.doi.org/10.1089/ten.tec.2018.0134] [PMID: 30101670]
[115]
Busche M, Tomilova O, Schütte J, et al. HepaChip-MP - a twenty-four chamber microplate for a continuously perfused liver coculture model. Lab Chip 2020; 20(16): 2911-26.
[http://dx.doi.org/10.1039/D0LC00357C] [PMID: 32662810]
[116]
Unal AZ, Jeffs SE, West JL. 3D co-culture with vascular cells supports long-term hepatocyte phenotype and function in vitro. Regen Eng Transl Med 2018; 4: 21-34.
[http://dx.doi.org/10.1007/s40883-018-0046-2]
[117]
Lu HF, Chua KN, Zhang PC, et al. Three-dimensional co-culture of rat hepatocyte spheroids and NIH/3T3 fibroblasts enhances hepatocyte functional maintenance. Acta Biomater 2005; 1(4): 399-410.
[http://dx.doi.org/10.1016/j.actbio.2005.04.003] [PMID: 16701821]

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