Bioartificial livers in vitro and in vivo: Tailoring biocomponents to the expanding variety of applications

Expert Opinion on Biological Therapy

Volumn 14, Issue 12, 2014, Pages 1745-1760

  Van Wenum, Martien ^a   Chamuleau, Robert Afm ^a   Van Gulik, Thomas M ^a   Siliakus, Adriaan ^a   Seppen, Jurgen ^a   Hoekstra, Ruurdtje ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Bioartificial liver; Drug induced liver injury; HepaRG; Hepatitis; Hepatocyte; Hepatocyte like cell; iHEP; Induced pluripotent stem cell; Liver; Stem cell

Indexed keywords

ALPHA FETOPROTEIN; AMMONIA; HEPATOCYTE NUCLEAR FACTOR; INTERLEUKIN 2 RECEPTOR; LACTIC ACID; PREGNANE X RECEPTOR; TRANSCRIPTION FACTOR; XENOBIOTIC AGENT;

ADULT STEM CELL; BIOARTIFICIAL LIVER; BIOREACTOR; CARBOHYDRATE METABOLISM; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TYPE; COCULTURE; COMPUTER; DATA BASE; DETOXIFICATION; DRUG TOXICITY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HEPATIC PROGENITOR CELL; HEPATOCYTE TRANSPLANTATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LIVER CELL; LIVER DEVELOPMENT; LIVER FUNCTION; LIVER TRANSPLANTATION; MEDLINE; NITROGEN METABOLISM; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN SYNTHESIS; REVIEW; STELLATE CELL; TUMOR MICROENVIRONMENT; ANIMAL; ARTIFICIAL LIVER; CELL CULTURE; CYTOLOGY; LIVER FAILURE; PHYSIOLOGY; PROCEDURES; STEM CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; HEPATOCYTES; HUMANS; IN VITRO TECHNIQUES; LIVER FAILURE; LIVER, ARTIFICIAL; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84910096805     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2014.950651     Document Type: Review

References (103)

1. Bernal W, Auzinger G, Dhawan A, Wendon J. Acute liver failure. Lancet 2010;376:190-201
2. Nibourg GA, Hoekstra R, van der Hoeven TV, et al. Increased hepatic functionality of the human hepatoma cell line HepaRG cultured in the AMC bioreactor. Int J Biochem Cell Biol 2013;45:1860-8
3. Selden C, Spearman CW, Kahn D, et al. Evaluation of encapsulated liver cell spheroids in a fluidised-bed bioartificial liver for treatment of ischaemic acute liver failure in pigs in a translational setting. PLoS One 2013;8:e82312
4. NCT01471028. 2011. Available from: www.clinicaltrials.gov
5. Godoy P, Hewitt NJ, Albrecht U, et al. Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Arch Toxicol 2013;87:1315-530
6. Giobbe GG, Tonon F, Zambon A, et al. Optimization of human pluripotent stem cell differentiation into hepatic cells under a stable microfluidic oxygen gradient. J Hepatol 2014;60:S102
7. Lee SA, No da Y, Kang E, et al. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab Chip 2013;13:3529-37
8. Van de Stolpe A, den Toonder J. Workshop meeting report Organs-on-Chips: human disease models. Lab Chip 2013;13:3449-70
9. Andria B, Bracco A, Cirino G, Chamuleau R. Liver cell culture devices. Cell Medicine 2010;1:55-70
10. Nibourg GA, Chamuleau RA, van Gulik TM, Hoekstra R. Proliferative human cell sources applied as biocomponent in bioartificial livers: a review. Expert Opin Biol Ther 2012;12:905-21 • A previous review by our group on proliferative hepatocyte sources applied as biocomponents in bioartificial livers.
11. Park JK, Lee DH. Bioartificial liver systems: current status and future perspective. J Biosci Bioeng 2005;99:311-19
12. Hanid MA, Davies M, Mellon PJ, et al. Clinical monitoring of intracranial pressure in fulminant hepatic failure. Gut 1980;21:866-9
13. Bernal W, Hyyrylainen A, Gera A, et al. Lessons from look-back in acute liver failure? A single centre experience of 3300 patients. J Hepatol 2013;59:74-80
14. Riordan SM, Williams R. Perspectives on liver failure: past and future. Semin Liver Dis 2008;28:137-41
15. Sekiyama KD, Yoshiba M, Thomson AW. Circulating proinflammatory cytokines (IL-1 beta, TNF-alpha, and IL-6) and IL-1 receptor antagonist (IL-1Ra) in fulminant hepatic failure and acute hepatitis. Clin Exp Immunol 1994;98:71-7
16. Rolando N, Wade J, Davalos M, et al. The systemic inflammatory response syndrome in acute liver failure. Hepatology 2000;32:734-9
17. Azoulay D, Samuel D, Ichai P, et al. Auxiliary partial orthotopic versus standard orthotopic whole liver transplantation for acute liver failure: a reappraisal from a single center by a case-control study. Ann Surg 2001;234:723-31
18. Chenard-Neu MP, Boudjema K, Bernuau J, et al. Auxiliary liver transplantation: regeneration of the native liver and outcome in 30 patients with fulminant hepatic failure - a multicenter European study. Hepatology 1996;23:1119-27
19. Tsiaoussis J, Newsome PN, Nelson LJ, et al. Which hepatocyte will it be? Hepatocyte choice for bioartificial liver support systems. Liver Transpl 2001;7:2-10
20. Eguchi S, Lilja H, Hewitt WR, et al. Loss and recovery of liver regeneration in rats with fulminant hepatic failure. J Surg Res 1997;72:112-22
21. Flendrig LM, la Soe JW, Jorning GG, et al. In vitro evaluation of a novel bioreactor based on an integral oxygenator and a spirally wound nonwoven polyester matrix for hepatocyte culture as small aggregates. J Hepatol 1997;26:1379-92
22. Erro E, Bundy J, Massie I, et al. Bioengineering the liver: scale-up and cool chain delivery of the liver cell biomass for clinical targeting in a bioartificial liver support system. Biores Open Access 2013;2:1-11
23. Hsu WM, Carraro A, Kulig KM, et al. Liver-assist device with a microfluidics-based vascular bed in an animal model. Ann Surg 2010;252:351-7
24. Hughes B. Industry concern over EU hepatotoxicity guidance. Nat Rev Drug Discov 2008;7:719
25. Russmann S, Kullak-Ublick GA, Grattagliano I. Current concepts of mechanisms in drug-induced hepatotoxicity. Curr Med Chem 2009;16:3041-53
26. Galinski MR, Meyer EV, Barnwell JW. Plasmodium vivax: modern strategies to study a persistent parasite's life cycle. Adv Parasitol 2013;81:1-26
27. Gondeau C, Pichard-Garcia L, Maurel P. Cellular models for the screening and development of anti-hepatitis C virus agents. Pharmacol Ther 2009;124:1-22
28. Tanner M, de Savigny D. Malaria eradication back on the table. Bull World Health Organ 2008;86:82
29. Dembele L, Franetich JF, Lorthiois A, et al. Persistence and activation of malaria hypnozoites in long-term primary hepatocyte cultures. Nat Med 2014;20:307-12
30. Meuleman P, Leroux-Roels G. The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res 2008;80:231-8
31. Allen JW, Khetani SR, Bhatia SN. In vitro zonation and toxicity in a hepatocyte bioreactor. Toxicol Sci 2005;84:110-19
32. Domansky K, Inman W, Serdy J, et al. Perfused multiwell plate for 3D liver tissue engineering. Lab Chip 2010;10:51-8
33. Takayama K, Kawabata K, Nagamoto Y, et al. 3D spheroid culture of hESC/hiPSC-derived hepatocyte-like cells for drug toxicity testing. Biomaterials 2013;34:1781-9
34. Nyberg SL, Hardin J, Amiot B, et al. Rapid, large-scale formation of porcine hepatocyte spheroids in a novel spheroid reservoir bioartificial liver. Liver Transpl 2005;11:901-10
35. Shen C, Zhang G, Qiu H, Meng Q. Acetaminophen-induced hepatotoxicity of gel entrapped rat hepatocytes in hollow fibers. Chem Biol Interact 2006;162:53-61
36. Carpentier B, Gautier A, Legallais C. Artificial and bioartificial liver devices: present and future. Gut 2009;58:1690-702
37. Carraro A, Hsu WM, Kulig KM, et al. In vitro analysis of a hepatic device with intrinsic microvascular-based channels. Biomed Microdevices 2008;10:795-805
38. Novik E, Maguire TJ, Chao P, et al. A microfluidic hepatic coculture platform for cell-based drug metabolism studies. Biochem Pharmacol 2010;79:1036-44
39. Jozefczuk J, Prigione A, Chavez L, Adjaye J. Comparative analysis of human embryonic stem cell and induced pluripotent stem cell-derived hepatocyte-like cells reveals current drawbacks and possible strategies for improved differentiation. Stem Cells Dev 2011;20:1259-75
40. Beigel J, Fella K, Kramer PJ, et al. Genomics and proteomics analysis of cultured primary rat hepatocytes. Toxicol In Vitro 2008;22:171-81
41. Baker TK, Carfagna MA, Gao H, et al. Temporal gene expression analysis of monolayer cultured rat hepatocytes. Chem Res Toxicol 2001;14:1218-31
42. Azuma H, Paulk N, Ranade A, et al. Robust expansion of human hepatocytes in Fah-/-/Rag2-/-/Il2rg-/- mice. Nat Biotechnol 2007;25:903-10
43. Burkard A, Dahn C, Heinz S, et al. Generation of proliferating human hepatocytes using Upcyte(R) technology: characterisation and applications in induction and cytotoxicity assays. Xenobiotica 2012;42:939-56
44. Seglen PO. Preparation of isolated rat liver cells. Methods Cell Biol 1976;13:29-83
45. OprodFraczek J, Bolleyn J, Vanhaecke T, et al. Primary hepatocyte cultures for pharmaco-toxicological studies: at the busy crossroad of various anti-dedifferentiation strategies. Arch Toxicol 2013;87:577-610 • Informative review on primary hepatocyte dedifferentiation and strategies to counter dedifferentiation.
46. Huang SM, Temple R, Throckmorton DC, Lesko LJ. Drug interaction studies: study design, data analysis, and implications for dosing and labeling. Clin Pharmacol Ther 2007;81:298-304
47. Guguen-Guillouzo C, Guillouzo A. General review on in vitro hepatocyte models and their applications. Methods Mol Biol 2010;640:1-40
48. Chamuleau RA, Deurholt T, Hoekstra R. Which are the right cells to be used in a bioartificial liver? Metab Brain Dis 2005;20:327-35
49. Yu LJ, Matias J, Scudiero DA, et al. P450 enzyme expression patterns in the NCI human tumor cell line panel. Drug Metab Dispos 2001;29:304-12
50. Nyberg SL, Remmel RP, Mann HJ, et al. Primary hepatocytes outperform Hep G2 cells as the source of biotransformation functions in a bioartificial liver. Ann Surg 1994;220:59-67
51. Mavri-Damelin D, Damelin LH, Eaton S, et al. Cells for bioartificial liver devices: the human hepatoma-derived cell line C3A produces urea but does not detoxify ammonia. Biotechnol Bioeng 2008;99:644-51 • This paper reports on the importance of distinguishing urea production from urea cycle activity.
52. Kia R, Sison RL, Heslop J, et al. Stem cell-derived hepatocytes as a predictive model for drug-induced liver injury: are we there yet? Br J Clin Pharmacol 2013;75:885-96
53. Banas A, Teratani T, Yamamoto Y, et al. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 2007;46:219-28
54. Kazemnejad S, Allameh A, Soleimani M, et al. Biochemical and molecular characterization of hepatocyte-like cells derived from human bone marrow mesenchymal stem cells on a novel three-dimensional biocompatible nanofibrous scaffold. J Gastroenterol Hepatol 2009;24:278-87
55. Fausto N. Liver regeneration and repair: hepatocytes, progenitor cells, and stem cells. Hepatology 2004;39:1477-87
56. Duret C, Gerbal-Chaloin S, Ramos J, et al. Isolation, characterization, and differentiation to hepatocyte-like cells of nonparenchymal epithelial cells from adult human liver. Stem Cells 2007;25:1779-90
57. Fonsato V, Herrera MB, Buttiglieri S, et al. Use of a rotary bioartificial liver in the differentiation of human liver stem cells. Tissue Eng Part C Methods 2010;16:123-32
58. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-72
59. McKernan R, Watt FM. What is the point of large-scale collections of human induced pluripotent stem cells? Nat Biotechnol 2013;31:875-7
60. Schwartz RE, Fleming HE, Khetani SR, Bhatia SN. Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv 2014;32(2):504-13
61. Schwartz RE, Trehan K, Andrus L, et al. Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci USA 2012;109:2544-8 • This paper describes the infection of iPCS-hepatocyte-like cell (HLC) with hepatitis C virus.
62. Rashid ST, Corbineau S, Hannan N, et al. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 2010;120:3127-36 • This paper demonstrates that iPS-HLCs can retain their donor hepatocyte phenotype.
63. Nagamoto Y, Tashiro K, Takayama K, et al. The promotion of hepatic maturation of human pluripotent stem cells in 3D co-culture using type I collagen and Swiss 3T3 cell sheets. Biomaterials 2012;33:4526-34
64. Yu Y, Liu H, Ikeda Y, et al. Hepatocyte-like cells differentiated from human induced pluripotent stem cells: relevance to cellular therapies. Stem Cell Res 2012;9:196-207
65. Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 2013;499:481-4
66. Hannan NR, Segeritz CP, Touboul T, Vallier L. Production of hepatocyte-like cells from human pluripotent stem cells. Nat Protoc 2013;8:430-7
67. Takayama K, Inamura M, Kawabata K, et al. Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4alpha transduction. Mol Ther 2012;20:127-37
68. Zhu S, Rezvani M, Harbell J, et al. Mouse liver repopulation with hepatocytes generated from human fibroblasts. Nature 2014;508(7494):93-7
69. Huang P, Zhang L, Gao Y, et al. Direct reprogramming of human fibroblasts to functional and expandable hepatocytes. Cell Stem Cell 2014;14:370-84 • One of two simultaneously published reports on direct lineage reprogramming of mesenchymal cells into HLCs.
70. Du Y, Wang J, Jia J, et al. Human hepatocytes with drug metabolic function induced from fibroblasts by lineage reprogramming. Cell Stem Cell 2014;14:394-403 • The second report on direct lineage reprogramming of mesenchymal cells into HLCs.
71. Roelandt P, Obeid S, Paeshuyse J, et al. Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus. J Hepatol 2012;57:246-51
72. Takayama K, Inamura M, Kawabata K, et al. Generation of metabolically functioning hepatocytes from human pluripotent stem cells by FOXA2 and HNF1alpha transduction. J Hepatol 2012;57:628-36
73. Song Z, Cai J, Liu Y, et al. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 2009;19:1233-42
74. Yagi H, Parekkadan B, Suganuma K, et al. Long-term superior performance of a stem cell/hepatocyte device for the treatment of acute liver failure. Tissue Eng Part A 2009;15:3377-88
75. Saito M, Matsuura T, Masaki T, et al. Reconstruction of liver organoid using a bioreactor. World J Gastroenterol 2006;12:1881-8
76. Dos Santos F, Campbell A, Fernandes-Platzgummer A, et al. A xenogeneic-free bioreactor system for the clinical-scale expansion of human mesenchymal stem/stromal cells. Biotechnol Bioeng 2014;111:1116-27
77. Cosgrove BD, King BM, Hasan MA, et al. Synergistic drug-cytokine induction of hepatocellular death as an in vitro approach for the study of inflammation-associated idiosyncratic drug hepatotoxicity. Toxicol Appl Pharmacol 2009;237:317-30
78. Parekkadan B, van Poll D, Suganuma K, et al. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS ONE 2007;2:e941
79. Sgroi A, Gonelle-Gispert C, Morel P, et al. Interleukin-1 receptor antagonist modulates the early phase of liver regeneration after partial hepatectomy in mice. PLoS ONE 2011;6:e25442
80. Shinoda M, Tilles AW, Wakabayashi G, et al. Treatment of fulminant hepatic failure in rats using a bioartificial liver device containing porcine hepatocytes producing interleukin-1 receptor antagonist. Tissue Eng 2006;12:1313-23
81. Taniguchi T. Cytokine adsorbing columns. Contrib Nephrol 2010;166:134-41
82. Bernal W, Hall C, Karvellas CJ, et al. Arterial ammonia and clinical risk factors for encephalopathy and intracranial hypertension in acute liver failure. Hepatology 2007;46:1844-52
83. Knudsen GM, Paulson OB, Hertz MM. Kinetic analysis of the human blood-brain barrier transport of lactate and its influence by hypercapnia. J Cereb Blood Flow Metab 1991;11:581-6
84. Bosoi CR, Zwingmann C, Marin H, et al. Increased brain lactate is central to the development of brain edema in rats with chronic liver disease. J Hepatol 2013;60(3):554-60 • This paper indicates a causal relation between lactate concentration and intracranial hypertension in rats.
85. Tofteng F, Jorgensen L, Hansen BA, et al. Cerebral microdialysis in patients with fulminant hepatic failure. Hepatology 2002;36:1333-40
86. Chen T, Qian YZ, Rice A, et al. Brain lactate uptake increases at the site of impact after traumatic brain injury. Brain Res 2000;861:281-7
87. Smith D, Pernet A, Hallett WA, et al. Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 2003;23:658-64
88. Oria M, Jalan R. Brain lactate in hepatic encephalopathy: Friend or foe? J Hepatol 2014;60(3):476-7
89. Wratten ML, Sereni L, Tetta C. Oxidation of albumin is enhanced in the presence of uremic toxins. Ren Fail 2001;23:563-71
90. Kouoh F, Gressier B, Luyckx M, et al. Antioxidant properties of albumin: effect on oxidative metabolism of human neutrophil granulocytes. Farmaco 1999;54:695-9
91. Arroyo V, Garcia-Martinez R, Salvatella X. Human serum albumin, systemic inflammation and cirrhosis. J Hepatol 2014;61(2):396-407
92. Wilhelm AJ, Zabalawi M, Owen JS, et al. Apolipoprotein A-I modulates regulatory T cells in autoimmune LDLr-/-, ApoA-I-/- mice. J Biol Chem 2010;285:36158-69
93. Etogo-Asse FE, Vincent RP, Hughes SA, et al. High density lipoprotein in patients with liver failure; relation to sepsis, adrenal function and outcome of illness. Liver Int 2012;32:128-36
94. Wang N, Tsuruoka S, Yamamoto H, et al. The bioreactor with CYP3A4- and glutamine synthetase-introduced HepG2 cells: treatment of hepatic failure dog with diazepam overdosage. Artif Organs 2005;29:681-4
95. Ahboucha S, Butterworth RF. Role of endogenous benzodiazepine ligands and their GABA-A-associated receptors in hepatic encephalopathy. Metab Brain Dis 2005;20:425-37
96. Enosawa S, Miyashita T, Saito T, et al. The significant improvement of survival times and pathological parameters by bioartificial liver with recombinant HepG2 in porcine liver failure model. Cell Transplant 2006;15:873-80
97. Guengerich FP. Cytochrome p450 and chemical toxicology. Chem Res Toxicol 2008;21:70-83
98. Oe S, Lemmer ER, Conner EA, et al. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice. Hepatology 2004;40:1098-105
99. Suh KS, Lilja H, Kamohara Y, et al. Bioartificial liver treatment in rats with fulminant hepatic failure: effect on DNA-binding activity of liver-enriched and growth-associated transcription factors. J Surg Res 1999;85:243-50
100. Zeilinger K, Schreiter T, Darnell M, et al. Scaling down of a clinical three-dimensional perfusion multicompartment hollow fiber liver bioreactor developed for extracorporeal liver support to an analytical scale device useful for hepatic pharmacological in vitro studies. Tissue Eng Part C Methods 2011;17:549-56
101. Darnell M, Ulvestad M, Ellis E, et al. In vitro evaluation of major in vivo drug metabolic pathways using primary human hepatocytes and HepaRG cells in suspension and a dynamic three-dimensional bioreactor system. J Pharmacol Exp Ther 2012;343:134-44
102. Si-Tayeb K, Noto FK, Nagaoka M, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010;51:297-305
103. Chen YF, Tseng CY, Wang HW, et al. Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology 2012;55:1193-203