Three dimensional cultures of rat liver cells using a natural self-assembling nanoscaffold in a clinically relevant bioreactor for bioartificial liver construction

Journal of Cellular Physiology

Volumn 227, Issue 1, 2012, Pages 313-327

  Giri, Shibashish ^a   Acikgöz, Ali ^a   Pathak, Priya ^a,b   Gutschker, Sylvia ^a   Kürsten, Anne ^a   Nieber, Karen ^a   Bader, Augustinus ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b Translational Centre for Regenerative Medicine (TRM Leipzig)   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ALANINE AMINOTRANSFERASE; ALBUMIN; AMMONIA; ASPARTATE AMINOTRANSFERASE; BONE MORPHOGENETIC PROTEIN 4; CYTOCHROME P450 3A1; DIAZEPAM; ERYTHROPOIETIN; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MOLECULAR SCAFFOLD; NORDAZEPAM; OXAZEPAM; SCATTER FACTOR; TEMAZEPAM; UREA;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BIOARTIFICIAL LIVER; BIOREACTOR; CELL MEMBRANE; CONTROLLED STUDY; DETOXIFICATION; DRUG TRANSFORMATION; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; LIVER CELL; MALE; MEMBRANE STABILIZATION; MITOCHONDRION; NONHUMAN; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; UREA CYCLE;

ANIMALS; BIOREACTORS; CELL CULTURE TECHNIQUES; LIVER, ARTIFICIAL; NANOTECHNOLOGY; RATS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

RATTUS;

EID: 80054945880     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22738     Document Type: Article

References (90)

1. Acikgoz A, Karim N, Giri S, Schmidt-Heck W, Bader A. 2009. Two compartment model of diazepam biotransformation in an organotypical culture of primary human hepatocytes. Toxicol Appl Pharmacol 234:179-191.
2. Bader A, Fruhauf N, Tiedge M, Drinkgern M, De Bartolo L, Borlak JT, Steinhoff G, Haverich A. 1999. Enhanced oxygen delivery reverses anaerobic metabolic states in prolonged sandwich rat hepatocyte culture. Exp Cell Res 246:221-232.
3. Basile AS, Hughes RD, Harrison PM, Murata Y, Pannell L, Jones EA, Williams R, Skolnick P. 1991. Elevated brain concentrations of 1, 4-benzodiazepines in fulminant hepatic failure. N Engl J Med 325:473-478.
4. Bernal W, Hall C, Karvellas CJ, Auzinger G, Sizer E, Wendon J. 2007. Arterial ammonia and clinical risk factors for encephalopathy and intracranial hypertension in acute liver failure. Hepatology 46:1844-1852.
5. Bhatia V, Singh R, Acharya SK. 2006. Predictive value of arterial ammonia for complications and outcome in acute liver failure. Gut 55:98-104.
6. Brophy CM, Luebke-Wheeler JL, Amiot BP, Khan H, Remmel RP, Rinaldo P, Nyberg SL. 2009. Rat hepatocyte spheroids formed by rocked technique maintain differentiated hepatocyte gene expression and function. Hepatology 49:578-586.
7. Brophy CM, Luebke-Wheeler JL, Amiot BP, Remmel RP, Rinaldo P, Nyberg SL. 2010. Gene expression and functional analyses of primary rat hepatocytes on nanofiber matrices. Cells Tissues Organs 191:129-140.
8. Calligaris SD, Almada LL, Guibert EE, Tiribelli C, Rodriguez JV. 2002. Ammonium detoxifying activity is maintained after 72hours of cold preservation of rat hepatocytes in University of Wisconsin (UW) solution. Cryo Lett 23:245-254.
9. Carpentier B, Gautier A, Legallais C. 2009. Artificial and bioartificial liver devices: present and future. Gut 58:1690-1702.
10. Chen HL, Chen CL, Huang TL, Chen TY, Tsang LL, Ou HY, Yu CY, Cheng YF. 2010. Regeneration rate of left liver grafts in adult living donor liver transplant. Transplant Proc 42:699-700.
11. Chen MF, Hwang TL, Hung CF. 1991. Human liver regeneration after major hepatectomy. A study of liver volume by computed tomography. Ann Surg 213:227-229.
12. Chen AA, Khetani SR, Lee S, Bhatia SN, Van Vliet KJ. 2009. Modulation of hepatocyte phenotype in vitro via chemomechanical tuning of polyelectrolyte multilayers. Biomaterials 30:1113-1120.
13. Chhabra R, Sharma J, Liu Y, Rinker S, Yan H. 2010. DNA Self-assembly for Nanomedicine. Adv Drug Deliv Rev 62:617-625.
14. Claudia R, Ballauff A, Lange R, Erhard J. 1997. Heterotopic auxiliary liver transplantation in a 3 year old boy with acute liver failure and aplastic anemia. Transplantation 64:658-660.
15. Cushing MC, Anseth KS. 2007. Materials science. Hydrogel cell cultures. Science 316:1133-1134.
16. De Bartolo L, Bader A. 2001. Review of a flat membrane bioreactor as a bioartificial liver. Ann Transplant 6:40-46.
17. Detry O, De Roover A, Honore P, Meurisse M. 2006. Brain edema and intracranial hypertension in fulminant hepatic failure: pathophysiology and manageme. World J Gastroenterol 12:7405-7412.
18. FDA (Food and Drug Administration), Center for Drug Evaluation and Research. August 2005. Guidance for Industry, Impurities in Drug Product. Revision I
19. Feng ZQ, Chu XH, Huang NP, Leach MK, Wang G, Wang YC, Ding YT, Gu ZZ. 2010. Rat hepatocyte aggregate formation on discrete aligned nanofibers of type-I collagen-coated poly(L-lactic acid). Biomaterials 31:3604-3612.
20. Frederick CB, Obach RS. 2010. Metabolites in safety testing: "MIST" for the clinical pharmacologist. Clin Pharmacol Ther 87:345-350.
21. Fruhauf NR, Oldhafer KJ, Holtje M, Kaiser GM, Fruhauf JH, Stavrou GA, Bader A, Broelsch CE. 2004. A bioartificial liver support system using primary hepatocytes: a preclinical study in a new porcine hepatectomy model. Surgery 136:47-56.
22. Fura A. 2006. Role of pharmacologically active metabolites in drug discovery and development. Drug Discov Today 11:133-142.
23. Giri S, Nieber K, Bader A. 2010. Hepatotoxicity and hepatic metabolism of available drugs: current problems and possible solutions in preclinical stages. Expert Opin Drug Metab Toxicol 6:895-917.
24. Green RM, Flamm S. 2002. AGA technical review on the evaluation of liver chemistry tests. Gastroenterology 123:1367-1384.
25. Goel A, Yadav S, Saraswat V, Srivastava A, Thomas MA, Pandey CM, Rathore R, Gupta R. 2010. Cerebral oedema in minimal hepatic encephalopathy due to extrahepatic portal venous obstruction. Liver Int 30:1143-1151.
26. Gouon-Evans V, Boussemart L, Gadue P, Nierhoff D, Koehler CI, Kubo A, Shafritz DA, Keller G. 2006. BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat Biotechnol 24:1402-1411.
27. Hay DC, Fletcher J, Payne C, Terrace JD, Gallagher RC, Snoeys J, Black JR, Wojtacha D, Samuel K, Hannoun Z, Pryde A, Filippi C, Currie IS, Forbes SJ, Ross JA, Newsome PN, Iredale JP. 2008. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci USA 105:12301-12306.
28. Holden A. Detecting and investigating drug-induced adverse events: the international serious Adverse event consortium's experience. 2008.
29. Howell CA, Sandeman SR, Phillips GJ, Lloyd AW, Davies JG, Mikhalovsky SV, Tennison SR, Rawlinson AP, Kozynchenko OP, Owen HL, Gaylor JD, Rouse JJ, Courtney JM. 2006. The in vitro adsorption of cytokines by polymer-pyrolysed carbon. Biomaterials 27:5286-5291.
30. Janorkar AV, Rajagopalan P, Yarmush ML, Megeed Z. 2008. The use of elastin-like polypeptide-polyelectrolyte complexes to control hepatocyte morphology and function in vitro. Biomaterials 29:625-632.
31. Jin X, Zhang Z, Beer-Stolz D, Zimmers TA, Koniaris LG. 2007. Interleukin-6 inhibits oxidative injury and necrosis after extreme liver resection. Hepatology 46:802-812.
32. Khetani SR, Bhatia SN. 2008. Microscale culture of human liver cells for drug development. Nat Biotechnol 26:120-126.
33. Kidambi S, Yarmush RS, Novik E, Chao P, Yarmush ML, Nahmias Y. 2009. Oxygen-mediated enhancement of primary hepatocyte metabolism, functional polarization, gene expression, and drug clearance. Proc Natl Acad Sci USA 106:15714-15719.
34. Kim M, Lee JY, Jones CN, Revzin A, Tae G. 2010. Heparin-based hydrogel as a matrix for encapsulation and cultivation of primary hepatocytes. Biomaterials 31:3596-3603.
35. Knowles SR, Uetrecht J, Shear NH. 2000. Shear, Idiosyncratic drug reactions: the reactive metabolite syndrome. Lancet 356:1587-1591.
36. Kundra A, Jain A, Banga A, Bajaj G, Kar P. 2005. Evaluation of plasma ammonia levels in patients with acute liver failure and chronic liver disease and its correlation with the severity of hepatic encephalopathy and clinical features of raised intracranial tension. Clin Biochem 38:696-699.
37. Lacour S, Gautier JC, Pallardy M, Roberts R. 2005. Cytokines as potential biomarkers of liver toxicity. Cancer Biomark 1:29-39.
38. Lee WM, Squires RH Jr, Nyberg SL, Doo E, Hoofnagle JH. 2008. Acute liver failure: summary of a workshop. Hepatology 47:1401-1415.
39. Lee JH, Choi YJ, Lim YB. 2010. Self-assembled filamentous nanostructures for drug/gene delivery applications. Expert Opin Drug Deliv 7:341-351.
40. Li Z, Leung M, Hopper R, Ellenbogen R, Zhang M. 2010. Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds. Biomaterials 31:404-412.
41. Liu J, Huang W, Pang Y, Zhu X, Zhou Y, Yan D. 2010. Self-assembled micelles from an amphiphilic hyperbranched copolymer with polyphosphate arms for drug delivery. Langmuir 26:10585-10592.
42. Luo JC, Cheng TJ, Kuo HW, Chang MJ. 2005. Abnormal liver function associated with occupational exposure to dimethylformamide and glutathione S-transferase polymorphisms. Biomarkers 10:464-474.
43. Maringka M, Giri S, Bader A. 2010. Preclinical characterization of primary porcine hepatocytes in a clinically relevant flat membrane bioreactor. Biomaterials 31:156-172.
44. Mallon BS, Park KY, Chen KG, Hamilton RS, McKay RD. 2006. Toward xeno-free culture of human embryonic stem cells. Int J Biochem Cell Biol 38:1063-1075.
45. Martin MJ, Muotri A, Gage F, Varki A. 2005. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 11:228-232.
46. McDermott WV Jr, Greenberger NJ, Isselbacher KJ, Weber AL. 1963. Major hepatic resection: diagnostic techniques and metabolic problems. Surgery 54:56-66.
47. Mehta G, Williams CM, Alvarez L, Lesniewski M, Kamm RD, Griffith LG. 2010. Synergistic effects of tethered growth factors and adhesion ligands on DNA synthesis and function of primary hepatocytes cultured on soft synthetic hydrogels. Biomaterials 31:4657-4671.
48. Millis JM, Losanoff JE. 2005. Technology insight: liver support systems. Nat Clin Pract Gastroenterol Hepatol 2:398-405, quiz 434.
49. Moriwaki H, Shiraki M, Iwasa J, Terakura Y. 2010. Hepatic encephalopathy as a complication of liver cirrhosis: an Asian perspective. J Gastroenterol Hepatol 25:858-863.
50. Nagino M, Ando M, Kamiya J, Uesaka K, Sano T, Nimura Y. 2001. Liver regeneration after major hepatectomy for biliary cancer. Br J Surg 88:1084-1091.
51. Nahmias Y, Kramvis Y, Barbe L, Casali M, Berthiaume F, Yarmush ML. 2006. A novel formulation of oxygen-carrying matrix enhances liver-specific function of cultured hepatocytes. FASEB J 20:2531-2533.
52. Papadopoulos N, Soultati A, Goritsas C, Lazaropoulou C, Achimastos A, Adamopoulos A, Dourakis SP. 2010. Nitric oxide, ammonia, and CRP levels in cirrhotic patients with hepatic encephalopathy: is there a connection? J Clin Gastroenterol 44:713-719.
53. Park B, Pirmohamed M, Kitteringham N. 1998. Role of drug disposition in drug hypersensitivity: a chemical, molecular, and clinical perspective. Chem Res Toxicol 11:969-988.
54. Pack GT, Islami AH, Hubbard JC, Brasfield RD. 1962. Regeneration of human liver after major hepatectomy. Surgery 52:617-623.
55. Palmes D, Spiegel HU. 2004. Animal models of liver regeneration. Biomaterials 25:1601-1611.
56. Parés A, Deulofeu R, Cisneros L, Escorsell A, Salmerón JM, Caballería J, Mas A. 2009. Albumin dialysis improves hepatic encephalopathy and decreases circulating phenolic aromatic amino acids in patients with alcoholic hepatitis and severe liver failure. Crit Care 13:R8.
57. Pavlica S, Piscioneri A, Peinemann F, Keller M, Milosevic J, Staeudte A, Heilmann A, Schulz-Siegmund M, Laera S, Favia P, De Bartolo L, Bader A. 2009. Rat embryonic liver cell expansion and differentiation on NH3 plasma-grafted PEEK-WC-PU membranes. Biomaterials 30:6514-6521.
58. Poyck PP, Mareels G, Hoekstra R, van Wijk AC, van der Hoeven TV, van Gulik TM, Verdonck PR, Chamuleau RA. 2008. Enhanced oxygen availability improves liver-specific functions of the AMC bioartificial liver. Artif Organs 32:116-126.
59. Quaglia A, Portmann BC, Knisely AS, Srinivasan P, Muiesan P, Wendon J, Heneghan MA, O'Grady JG, Samyn M, Hadzic D, Dhawan A, Mieli-Vergani G, Heaton N, Rela M. 2008. Auxiliary transplantation for acute liver failure: histopathological study of native liver regeneration. Liver Transpl 14:1437-1448.
60. Rozga J, Podesta L, LePage E, Hoffman A, Morsiani E, Sher L, Woolf GM, Makowka L, Demetriou AA. 1993. Control of cerebral oedema by total hepatectomy and extracorporeal liver support in fulminant hepatic failure. Lancet 342:898-899.
61. Saha K, Pollock JF, Schaffer DV, Healy KE. 2007. Designing synthetic materials to control stem cell phenotype. Curr Opin Chem Biol 11:381-387.
62. Schafer DF, Sorrell MF. 1997. Power failure, liver failure. N Engl J Med 336:1173-1174.
63. Schmeding M, Boas-Knoop S, Lippert S, Ruehl M, Somasundaram R, Dagdelen T, Neuhaus P, Neumann UP. 2008. Erythropoietin promotes hepatic regeneration after extended liver resection in rats. J Gastroenterol Hepatol 23:1125-1131.
64. Schmitmeier S, Langsch A, Jasmund I, Bader A. 2006. Development and characterization of a small-scale bioreactor based on a bioartificial hepatic culture model for predictive pharmacological in vitro screenings. Biotechnol Bioeng 95:1198-1206.
65. Scott MR, Will R, Ironside J, Nguyen HO, Tremblay P, DeArmond SJ, Prusiner SB. 1999. Compelling transgenetic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc Natl Acad Sci USA 96:15137-15142.
66. Shi Q, Hong H, Senior J, Tong W. 2010. Biomarkers for drug-induced liver injury. Expert Rev Gastroenterol Hepatol 4:225-234.
67. Singhvi R, Kumar A, Lopez GP, Stephanopoulos GN, Wang DI, Whitesides GM, Ingber DE. 1994. Engineering cell shape and function. Science 264:696-698.
68. Sotil EU, Gottstein J, Ayala E, Randolph C, Blei AT. 2009. Impact of preoperative overt hepatic encephalopathy on neurocognitive function after liver transplantation. Liver Transpl 15:184-192.
69. Stevens KM. 1965. Oxygen requirements for liver cells in vitro. Nature 206:199.
70. Stefanovich P, Matthew HW, Toner M, Tompkins RG, Yarmush ML. 1996. Extracorporeal plasma perfusion of cultured hepatocytes: effect of intermittent perfusion on hepatocyte function and morphology. J Surg Res 66:57-563.
71. Sugimoto H, Yang C, LeBleu VS, Soubasakos MA, Giraldo M, Zeisberg M, Kalluri R. 2007. BMP-7 functions as a novel hormone to facilitate liver regeneration. FASEB J 21:256-264.
72. Sulzbacher S, Schroeder IS, Truong TT, Wobus AM. 2009. Activin A-induced differentiation of embryonic stem cells into endoderm and pancreatic progenitors-the influence of differentiation factors and culture conditions. Stem Cell Rev 5:159-173.
73. Taub R. 2004. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 5:836-847.
74. Teperman LW, Peyregne VP. 2010. Considerations on the impact of hepatic encephalopathy treatments in the pretransplant setting. Transplantation 89:771-778.
75. Temple RJ. Hepatoxicity through the years: impact on the FDA. (Accessed January 20, 2006, at
76. Tiberio GA, Tiberio L, Benetti A, Cervi E, Montani N, Dreano M, Garotta G, Cerea K, Steimberg N, Pandolfo G, Ferrari-Bravo A, Mazzoleni G, Giulini SM, Schiaffonati L. 2008. IL-6 Promotes compensatory liver regeneration in cirrhotic rat after partial hepatectomy. Cytokine 42:372-378.
77. Ueki T, Kaneda Y, Tsutsui H, Nakanishi K, Sawa Y, Morishita R, Matsumoto K, Nakamura T, Takahashi H, Okamoto E, Fujimoto J. 1999. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat Med 5:226-230.
78. van Anken HC, Schiphorst ME. 1974. A kinetic determination of ammonia in plasma. Clin Chim Acta 56:151-157.
79. van de Kerkhove MP, Hoekstra R, Chamuleau RA, van Gulik TM. 2004. Clinical application of bioartificial liver support systems. Ann Surg 240:216-230.
80. Vonarbourg A, Passirani C, Desigaux L, Allard E, Saulnier P, Lambert O, Benoit JP, Pitard B. 2009. The encapsulation of DNA molecules within biomimetic lipid nanocapsules. Biomaterials 30:3197-3204.
81. Vukicevic S, Latin V, Chen P, Batorsky R, Reddi AH, Sampath TK. 1994. Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes. Biochem Biophys Res Commun 198:693-700.
82. Walgren JL, Mitchell MD, Thompson DC. 2005. Role of metabolism in drug-induced idiosyncratic hepatotoxicity. Crit Rev Toxicol 35:325-361.
83. Xu C, He JQ, Kamp TJ, Police S, Hao X, O'Sullivan C, Carpenter MK, Lebkowski J, Gold JD. 2006. Human embryonic stem cell-derived cardiomyocytes can be maintained in defined medium without serum. Stem Cells Dev 15:931-941.
84. Yokoi H, Kinoshita T, Zhang S. 2005. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc Natl Acad Sci USA 102:8414-8419.
85. Zhang S. 2003. Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21:1171-1178.
86. Zhang S. 2004. Beyond the Petri dish. Nat Biotechnol 22:151-152.
87. Zhang S, Lockshin C, Herbert A, Winter E, Rich A. 1992. Zuotin, a putative Z-DNA binding protein in Saccharomyces cerevisiae. EMBO J 11:3787-3796.
88. Zhang S, Holmes T, Lockshin C, Rich A. 1993. Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc Natl Acad Sci USA 90:3334-3338.
89. Zhang S, Lockshin C, Cook R, Rich A. 1994. Unusually stable beta-sheet formation in an ionic self-complementary oligopeptide. Biopolymers 34:663-672.
90. Zhong Q, Chinta DM, Pamujula S, Wang H, Yao X, Mandal TK, Luftig RB. 2010. Optimization of DNA delivery by three classes of hybrid nanoparticle/DNA complexes. J Nanobiotechnol 8:6.