Featured Article: Isolation, characterization, and cultivation of human hepatocytes and non-parenchymal liver cells

Experimental Biology and Medicine

Volumn 240, Issue 5, 2015, Pages 645-656

  Pfeiffer, Elisa ^a   Kegel, Victoria ^a   Zeilinger, Katrin ^a   Hengstler, Jan G ^b   Nüssler, Andreas K ^c   Seehofer, Daniel ^a   Damm, Georg ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b LEIBNIZ RESEARCH CENTRE FOR WORKING ENVIRONMENT AND HUMAN FACTORS   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Liver; liver in vitro model; liver tissue engineering; non parenchymal liver cells; primary cell isolation; primary human hepatocytes

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD68 ANTIGEN; LIPOPROTEIN; MATRIX PROTEIN; RETINOL; VIMENTIN;

ARTICLE; CELL ACTIVATION; CELL FATE; CELL FRACTIONATION; CELL ISOLATION; CELL PHAGOCYTOSIS; CELL PROLIFERATION; CELL SELECTION; CELL SEPARATION; CELL VIABILITY; COLORIMETRY; ENDOTHELIUM CELL; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KUPFFER CELL; LIVER CELL; MYOFIBROBLAST; PINOCYTOSIS; SCANNING ELECTRON MICROSCOPY; STELLATE CELL; XTT ASSAY; CELL ADHESION; CELL CULTURE; CYTOLOGY; LIVER; PHAGOCYTOSIS;

CELL ADHESION; CELLS, CULTURED; HEPATOCYTES; HUMANS; LIVER; MICROSCOPY, ELECTRON, SCANNING; PHAGOCYTOSIS;

EID: 84930464270     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370214558025     Document Type: Article

References (41)

1. Si-Tayeb K,Lemaigre FP,Duncan SA.Organogenesis and development of the liver.Dev Cell. 2010;18:175-89
2. Godoy P,Hewitt NJ,Albrecht U,Andersen ME,Ansari N,Bhattacharya S,Bode JG,Bolleyn J,Borner C,Bottger J,Braeuning A,Budinsky RA,Burkhardt B,Cameron NR,Camussi G,Cho CS,Choi YJ,Craig Rowlands J,Dahmen U,Damm G,Dirsch O,Donato MT,Dong J,Dooley S,Drasdo D,Eakins R,Ferreira KS,Fonsato V,Fraczek J,Gebhardt R,Gibson A,Glanemann M,Goldring CE,Gomez-Lechon MJ,Groothuis GM,Gustavsson L,Guyot C,Hallifax D,Hammad S,Hayward A,Haussinger D,Hellerbrand C,Hewitt P,Hoehme S,Holzhutter HG,Houston JB,Hrach J,Ito K,Jaeschke H,Keitel V,Kelm JM,Kevin Park B,Kordes C,Kullak-Ublick GA,LeCluyse EL,Lu P,Luebke-Wheeler J,Lutz A,Maltman DJ,Matz-Soja M,McMullen P,Merfort I,Messner S,Meyer C,Mwinyi J,Naisbitt DJ,Nussler AK,Olinga P,Pampaloni F,Pi J,Pluta L,Przyborski SA,Ramachandran A,Rogiers V,Rowe C,Schelcher C,Schmich K,Schwarz M,Singh B,Stelzer EH,Stieger B,Stober R,Sugiyama Y,Tetta C,Thasler WE,Vanhaecke T,Vinken M,Weiss TS,Widera A,Woods CG,Xu JJ,Yarborough KM,Hengstler JG.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
3. Wisse E,Braet F,Luo D,De Zanger R,Jans D,Crabbe E,Vermoesen A.Structure and function of sinusoidal lining cells in the liver.Toxicol Pathol. 1996;24:100-11
4. Bilzer M,Roggel F,Gerbes AL.Role of Kupffer cells in host defense and liver disease.Liver Int. 2006;26:1175-86
5. Kmiec Z.Cooperation of liver cells in health and disease.Adv Anat Embryol Cell Biol. 2001;161:1–151.
6. Gandhi CMolecular pathology of liver diseases Molecular Pathology Library. Monga SPS, ed. USA: Springer; 2011:81-95.
7. Kolios G,Valatas V,Kouroumalis E.Role of Kupffer cells in the pathogenesis of liver disease.World J Gastroenterol. 2006;12:7413-20
8. Sumpio BE,Riley JT,Dardik A.Cells in focus: endothelial cell.Int J Biochem Cell Biol. 2002;34:1508-12
9. Kim Y,Rajagopalan P.3D hepatic cultures simultaneously maintain primary hepatocyte and liver sinusoidal endothelial cell phenotypes.PLoS One. 2010;5:e15456-e15456
10. Tokairin T,Nishikawa Y,Doi Y,Watanabe H,Yoshioka T,Su M,Omori Y,Enomoto K.A highly specific isolation of rat sinusoidal endothelial cells by the immunomagnetic bead method using SE-1 monoclonal antibody.J Hepatol. 2002;36:725-33
11. Elvevold K,Smedsrod B,Martinez I.The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity.Am J Physiol Gastrointest Liver Physiol. 2008;294:G391-400
12. March S,Hui EE,Underhill GH,Khetani S,Bhatia SN.Microenvironmental regulation of the sinusoidal endothelial cell phenotype in vitro.Hepatology. 2009;50:920-8
13. Hellerbrand C.Hepatic stellate cells–the pericytes in the liver.Pflugers Arch. 2013;465:775-8
14. Friedman SL.Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver.Physiol Rev. 2008;88:125-72
15. Asahina K.Hepatic stellate cell progenitor cells.J Gastroenterol Hepatol. 2012;27:80-4
16. Kocabayoglu P,Friedman SL.Cellular basis of hepatic fibrosis and its role in inflammation and cancer.Front Biosci (Schol Ed). 2013;5:217-30
17. Yin C,Evason KJ,Asahina K,Stainier DY.Hepatic stellate cells in liver development, regeneration, and cancer.J Clin Invest. 2013;123:1902-10
18. Gómez-Lechón MJ,Catell JV,Donato MT.Hepatocytes – the choice to investigate drug metabolism and toxicity in man: In vitro variability as a reflection of in vivo.Chem-Biol Interact. 2007;168:30-50
19. Ginai M,Elsby R,Hewitt CJ,Surry D,Fenner K,Coopman K.The use of bioreactors as in vitro models in pharmaceutical research.Drug Discov Today. 2013;18:922-35
20. Kasuya J,Sudo R,Mitaka T,Ikeda M,Tanishita K.Hepatic stellate cell-mediated three-dimensional hepatocyte and endothelial cell triculture model.Tissue Eng Part A. 2011;17:361-70
21. Kostadinova R,Boess F,Applegate D,Suter L,Weiser T,Singer T,Naughton B,Roth A.A long-term three dimensional liver co-culture system for improved prediction of clinically relevant drug-induced hepatotoxicity.Toxicol Appl Pharmacol. 2013;268:1-16
22. Messner S,Agarkova I,Moritz W,Kelm JM.Multi-cell type human liver microtissues for hepatotoxicity testing.Arch Toxicol. 2013;87:209-13
23. Friedman SL,Roll FJ.Isolation and culture of hepatic lipocytes, Kupffer cells, and sinusoidal endothelial cells by density gradient centrifugation with Stractan.Anal Biochem. 1987;161:207-18
24. Knook DL,Blansjaar N,Sleyster EC.Isolation and characterization of Kupffer and endothelial cells from the rat liver.Exp Cell Res. 1977;109:317-29
25. Alabraba EB,Curbishley SM,Lai WK,Wigmore SJ,Adams DH,Afford SC.A new approach to isolation and culture of human Kupffer cells.J Immunol Meth. 2007;326:139-44
26. Friedman SL,Rockey DC,McGuire RF,Maher JJ,Boyles JK,Yamasaki G.Isolated hepatic lipocytes and Kupffer cells from normal human liver: morphological and functional characteristics in primary culture.Hepatology. 1992;15:234-43
27. 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;12:5429-39
28. Damm G,Pfeiffer E,Burkhardt B,Vermehren J,Nüssler AK,Weiss TS.Human parenchymal and non-parenchymal liver cell isolation, culture and characterization.Hepatol Int. 2013;7:951-8
29. Rajan N,Habermehl J,Cote MF,Doillon CJ,Mantovani D.Preparation of ready-to-use, storable and reconstituted type I collagen from rat tail tendon for tissue engineering applications.Nat Protoc. 2006;1:2753-8
30. Nüssler AK, Nüssler NC, Merk V, Brulport M, Schormann W, Yao P, Hengstler JG. The Holy Grail of Hepatocyte Culturing and Therapeutic Use. In: Santin M (ed.) Strategies in regenerative Medicine, 2009.
31. Hosomura N,Kono H,Tsuchiya M,Ishii K,Ogiku M,Matsuda M,Fujii H.HCV-related proteins activate Kupffer cells isolated from human liver tissues.Dig Dis Sci. 2011;56:1057-64
32. Chang W,Yang M,Song L,Shen K,Wang H,Gao X,Li M,Niu W,Qin X.Isolation and culture of hepatic stellate cells from mouse liver.Acta Biochim Biophys Sin (Shanghai). 2014;46:291-8
33. Zeng WQ,Zhang JQ,Li Y,Yang K,Chen YP,Liu ZJ.A new method to isolate and culture rat kupffer cells.PLoS One. 2013;8:e70832-e70832
34. Kitani H,Takenouchi T,Sato M,Yoshioka M,Yamanaka N.A novel isolation method for macrophage-like cells from mixed primary cultures of adult rat liver cells.J Immunol Meth. 2010;360:47-55
35. Gerlach JC,Zeilinger K,Spatkowski G,Hentschel F,Schnoy N,Kolbeck S,Schindler RK,Neuhaus P.Large-scale isolation of sinusoidal endothelial cells from pig and human liver.J Surg Res. 2001;100:39-45
36. Liu T,Guevara OE,Warburton RR,Hill NS,Gaestel M,Kayyali US.Regulation of vimentin intermediate filaments in endothelial cells by hypoxia.Am J Physiol Cell Physiol. 2010;299:C363-73
37. DeLeve LD,Wang X,McCuskey MK,McCuskey RS.Rat liver endothelial cells isolated by anti-CD31 immunomagnetic separation lack fenestrae and sieve plates.Am J Physiol Gastrointest Liver Physiol. 2006;291:G1187-9
38. Olsen AL,Bloomer SA,Chan EP,Gaca MD,Georges PC,Sackey B,Uemura M,Janmey PA,Wells RG.Hepatic stellate cells require a stiff environment for myofibroblastic differentiation.Am J Physiol Gastrointest Liver Physiol. 2011;301:G110-8
39. Gaca MD,Zhou X,Issa R,Kiriella K,Iredale JP,Benyon RC.Basement membrane-like matrix inhibits proliferation and collagen synthesis by activated rat hepatic stellate cells: evidence for matrix-dependent deactivation of stellate cells.Matrix Biol. 2003;22:229-39
40. Schyschka L,Sanchez JJ,Wang Z,Burkhardt B,Muller-Vieira U,Zeilinger K,Bachmann A,Nadalin S,Damm G,Nussler AK.Hepatic 3D cultures but not 2D cultures preserve specific transporter activity for acetaminophen-induced hepatotoxicity.Arch Toxicol. 2013;87:1581-93
41. Zeilinger K,Schreiter T,Darnell M,Soderdahl T,Lubberstedt M,Dillner B,Knobeloch D,Nussler AK,Gerlach JC,Andersson TB.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 Meth. 2011;17:549-56