All-in-one: Advanced preparation of human parenchymal and non-parenchymal liver cells

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Werner, Melanie ^a   Driftmann, Sabrina ^a   Kleinehr, Kathrin ^a   Kaiser, Gernot M ^a   Mathé, Zotlan ^a,b   Treckmann, Juergen Walter ^a   Paul, Andreas ^a   Skibbe, Kathrin ^a   Timm, Joerg ^a,c   Canbay, Ali ^a   Gerken, Guido ^a   Schlaak, Joerg F ^a   Broering, Ruth ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA SMOOTH MUSCLE ACTIN; CD146 ANTIGEN; CD68 ANTIGEN; CYTOCHROME P450; LOW DENSITY LIPOPROTEIN; RETINOL; BIOLOGICAL MARKER;

ARTICLE; CELL COUNT; CELL FUNCTION; CELL ISOLATION; CELL POPULATION; CELL SELECTION; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; KUPFFER CELL; LIVER CELL; PHAGOCYTOSIS; PROTEIN EXPRESSION; SINGLE CELL ANALYSIS; STELLATE CELL; CELL SEPARATION; CYTOLOGY; HEPATIC STELLATE CELL; LIVER; METABOLISM; PRIMARY CELL CULTURE;

BIOMARKERS; CELL SEPARATION; ENDOTHELIAL CELLS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; KUPFFER CELLS; LIVER; PRIMARY CELL CULTURE;

EID: 84947724420     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138655     Document Type: Article

References (63)

1. Jungermann K. Zonation of metabolism and gene expression in liver. Histochem Cell Biol 1995; 103:81-91. PMID: 7634156
2. Kmiec Z. Cooperation of liver cells in health and disease. Adv Anat Embryol Cell Biol 2001; 161:III-XIII, 1-151. PMID: 11729749
3. McCuskey R. Anatomy of the liver. In: Boyer TD, Manns MP, Sanyal AJ, editors. Zakim and Boyer's Hepatology: a textbook of liver disease. Philadelphia, Pennsylvania, USA: Elsevier Sciences; 2012. p. 3-19.
4. Blouin A, Bolender RP, Weibel ER. Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study. J Cell Biol 1977; 72:441-455. PMID: 833203
5. Wisse E, van't Noordende JM, van der Meulen J, Daems WT. The pit cell: description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res 1976; 173:423-435. PMID: 991252
6. Smedsrod B, De Bleser PJ, Braet F, Lovisetti P, Vanderkerken K, Wisse E et al. Cell biology of liver endothelial and Kupffer cells. Gut 1994; 35:1509-1516. PMID: 7828963
7. Kolios G, Valatas V, Kouroumalis E. Role of Kupffer cells in the pathogenesis of liver disease. World J Gastroenterol 2006; 12:7413-7420. PMID: 17167827
8. Bouwens L, Baekeland M, De Zanger R, Wisse E. Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 1986; 6:718-722. PMID: 3733004
9. Roberts R A, Ganey PE, Ju C, Kamendulis LM, Rusyn I, Klaunig JE. Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis. Toxicol Sci 2007; 96:2-15. PMID: 17122412
10. Clavien P A, Camargo CA Jr, Cameron R, Washington MK, Phillips MJ, Greig PD et al. Kupffer cell erythrophagocytosis and graft-versus-host hemolysis in liver transplantation. Gastroenterology 1996; 110:1891-1896. PMID: 8964415
11. Dini L, Pagliara P, Carla EC. Phagocytosis of apoptotic cells by liver: a morphological study. Microsc Res Tech 2002; 57:530-540. PMID: 12112436
12. Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp Hepatol 2002; 1:1. PMID: 12437787
13. Elvevold K H, Nedredal GI, Revhaug A, Smedsrod B. Scavenger properties of cultivated pig liver endothelial cells. Comp Hepatol 2004; 3:1-11.
14. Friedman S L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008; 88:125-172. doi: 10.1152/physrev.00013.2007 PMID: 18195085
15. Kupffer Cv. Ueber Sternzellen der Leber. Archiv für Mikroskopische Anatomie 1876; 12:353-358.
16. Moreira R K. Hepatic stellate cells and liver fibrosis. Arch Pathol Lab Med 2007; 131:1728-1734. PMID: 17979495
17. Tacke F, Weiskirchen R. Update on hepatic stellate cells: pathogenic role in liver fibrosis and novel isolation techniques. Expert Rev Gastroenterol Hepatol 2012; 6:67-80. doi: 10.1586/egh.11.92 PMID: 22149583
18. Tiegs G, Lohse AW. Immune tolerance: what is unique about the liver. J Autoimmun 2010; 34:1-6. doi: 10.1016/j.jaut.2009.08.008 PMID: 19717280
19. Lalor P F, 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; 12:5429-5439. PMID: 17006978
20. Liu Z X, Kaplowitz N. Role of innate immunity in acetaminophen-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2006; 2:493-503. PMID: 16859400
21. Godoy P, Hewitt NJ, Albrecht U, Andersen ME, Ansari N, Bhattacharya S 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; 87:1315-1530. doi: 10.1007/s00204-013-1078-5 PMID: 23974980
22. Seglen P O. Preparation of isolated rat liver cells. Methods Cell Biol 1976; 13:29-83. PMID: 177845
23. Alabraba E B, Curbishley SM, Lai WK, Wigmore SJ, Adams DH, Afford SC. A new approach to isolation and culture of human Kupffer cells. J Immunol Methods 2007; 326:139-144. PMID: 17692868
24. Braet F, De Zanger R, Sasaoki T, Baekeland M, Janssens P, Smedsrod B et al. Assessment of a method of isolation, purification, and cultivation of rat liver sinusoidal endothelial cells. Lab Invest 1994; 70:944-952. PMID: 8015298
25. Bhogal R H, Hodson J, Bartlett DC, Weston CJ, Curbishley SM, Haughton E et al. Isolation of primary human hepatocytes from normal and diseased liver tissue: a one hundred liver experience. PLoS One 2011; 6:e18222. doi: 10.1371/journal.pone.0018222 PMID: 21479238
26. Chang W, Yang M, Song L, Shen K, Wang H, Gao X et al. Isolation and culture of hepatic stellate cells from mouse liver. Acta Biochim Biophys Sin (Shanghai) 2014; 46:291-298.
27. Pfeiffer E, Kegel V, Zeilinger K, Hengstler JG, Nussler AK, Seehofer D, et al. Isolation, characterization, and cultivation of human hepatocytes and non-parenchymal liver cells. Exp Biol Med (Maywood). 2015; 240: 645-656.
28. Bustin S A, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009; 55:611-622. doi: 10.1373/clinchem.2008.112797 PMID: 19246619
29. McCune J S, Hawke RL, LeCluyse EL, Gillenwater HH, Hamilton G, Ritchie J et al. In vivo and in vitro induction of human cytochrome P4503A4 by dexamethasone. Clin Pharmacol Ther 2000; 68:356-366. PMID: 11061575
30. Hubbard A L, Wilson G, Ashwell G, Stukenbrok H. An electron microscope autoradiographic study of the carbohydrate recognition systems in rat liver. I. Distribution of 125I-ligands among the liver cell types. J Cell Biol 1979; 83:47-64. PMID: 511941
31. Hubbard A L, Stukenbrok H. An electron microscope autoradiographic study of the carbohydrate recognition systems in rat liver. II. Intracellular fates of the 125I-ligands. J Cell Biol 1979; 83:65-81. PMID: 511942
32. Stockert R J. The asialoglycoprotein receptor: relationships between structure, function, and expression. Physiol Rev 1995; 75:591-609. PMID: 7624395
33. Mason T M. The role of factors that regulate the synthesis and secretion of very-low-density lipoprotein by hepatocytes. Crit Rev Clin Lab Sci 1998; 35:461-487. PMID: 9885772
34. Dixon J L, Ginsberg HN. Regulation of Hepatic Secretion of Apolipoprotein B-Containing Lipoproteins-Information obtained from Cultured Liver-Cells. J Lipid Res 1993; 34:167-179. PMID: 8381452
35. Lacroix D, Sonnier M, Moncion A, Cheron G, Cresteil T. Expression of CYP3A in the human liver-evidence that the shift between CYP3A7 and CYP3A4 occurs immediately after birth. Eur J Biochem 1997; 247:625-634. PMID: 9266706
36. Daneker GW, Lund SA, Caughman SW, Swerlick RA, Fischer AH, Staley CA et al. Culture and characterization of sinusoidal endothelial cells isolated from human liver. In Vitro Cell Dev Biol Anim 1998; 34:370-377. PMID: 9639099
37. 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. PMID: 18063708
38. Li R, Oteiza A, Sorensen KK, McCourt P, Olsen R, Smedsrod B et al. Role of liver sinusoidal endothelial cells and stabilins in elimination of oxidized low-density lipoproteins. Am J Physiol Gastrointest Liver Physiol 2011; 300:G71-81. doi: 10.1152/ajpgi.00215.2010 PMID: 21030611
39. Sato M, Suzuki S, Senoo H. Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 2003; 28:105-112. PMID: 12808230
40. Cassiman D, Libbrecht L, Desmet V, Denef C, Roskams T. Hepatic stellate cell/myofibroblast subpopulations in fibrotic human and rat livers. J Hepatol 2002; 36:200-209. PMID: 11830331
41. Kawai S, Enzan H, Hayashi Y, Jin YL, Guo LM, Miyazaki E et al. Vinculin: a novel marker for quiescent and activated hepatic stellate cells in human and rat livers. Virchows Arch 2003; 443:78-86. PMID: 12719976
42. Wake K. "Sternzellen" in the liver: perisinusoidal cells with special reference to storage of vitamin A. Am J Anat 1971; 132:429-462. PMID: 4942297
43. Mezaki Y, Morii M, Hebiguchi T, Yoshikawa K, Yamaguchi N, Yoshino H et al. The role of retinoic acid receptors in activated hepatic stellate cells. Med Hypotheses 2013; 81:222-224. doi: 10.1016/j.mehy. 2013.04.045 PMID: 23688744
44. D'Ambrosio DN, Walewski JL, Clugston RD, Berk PD, Rippe RA, Blaner WS. Distinct populations of hepatic stellate cells in the mouse liver have different capacities for retinoid and lipid storage. PLoS One. 2011; 6: e24993. doi: 10.1371/journal.pone.0024993 PMID: 21949825
45. Motoyama H, Komiya T, Thuy Le Thi Thanh, Tamori A, Enomoto M, Morikawa H et al. Cytoglobin is expressed in hepatic stellate cells, but not in myofibroblasts, in normal and fibrotic human liver. Laboratory Investigation 2014; 94:192-207. doi: 10.1038/labinvest.2013.135 PMID: 24296877
46. Knook DL, Seffelaar AM, de Leeuw AM. Fat-storing cells of the rat liver. Their isolation and purification. Exp Cell Res 1982; 139:468-471. PMID: 7084333
47. Valatas V, Xidakis C, Roumpaki H, Kolios G, Kouroumalis EA. Isolation of rat Kupffer cells: a combined methodology for highly purified primary cultures. Cell Biol Int 2003; 27:67-73. PMID: 12713802
48. Ikejima K, Enomoto N, Seabra V, Ikejima A, Brenner DA, Thurman RG. Pronase destroys the lipopolysaccharide receptor CD14 on Kupffer cells. Am J Physiol 1999; 276:G591-8. PMID: 10070034
49. Heinzelmann M, Bosshart H. Heparin binds to lipopolysaccharide (LPS)-binding protein, facilitates the transfer of LPS to CD14, and enhances LPS-induced activation of peripheral blood monocytes. J Immunol 2005; 174:2280-2287. PMID: 15699163
50. ZengWQ, 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. doi: 10.1371/journal.pone.0070832 PMID: 23967115
51. Irving M G, Roll FJ, Huang S, Bissell DM. Characterization and culture of sinusoidal endothelium from normal rat liver: lipoprotein uptake and collagen phenotype. Gastroenterology 1984; 87:1233-1247. PMID: 6092194
52. Kordes C, Sawitza I, Muller-Marbach A, Ale-Agha N, Keitel V, Klonowski-Stumpe H et al. CD133+ hepatic stellate cells are progenitor cells. Biochem Biophys Res Commun 2007; 352:410-417. PMID: 17118341
53. Beilfuss A, Sowa JP, Sydor S, Beste M, Bechmann LP, Schlattjan M et al. Vitamin D counteracts fibrogenic TGF-beta signalling in human hepatic stellate cells both receptor-dependently and independently. Gut 2014.
54. Mederacke I, Dapito DH, Affo S, Uchinami H, Schwabe RF. High-yield and high-purity isolation of hepatic stellate cells from normal and fibrotic mouse livers. Nature Protocols 2015; 10:305-315. doi: 10.1038/nprot.2015.017 PMID: 25612230
55. Laba A, Ostrowska A, Patrzalek D, Paradowski L, Lange A. Characterization of human hepatocytes isolated from non-transplantable livers. Arch Immunol Ther Exp (Warsz). 2005; 53: 442-453.
56. Gerlach JC, Zeilinger K, Spatkowski G, Hentschel F, Schnoy N, Kolbeck S, et al. Large-scale isolation of sinusoidal endothelial cells from pig and human liver. J Surg Res. 2001; 100: 39-45. PMID: 11516203
57. Nakamura A, Ueno T, Yagi Y, Okuda K, Ogata T, Nakamura T, et al. Human primary cultured hepatic stellate cells can be cryopreserved. Med Mol Morphol. 2010; 43: 107-115. doi: 10.1007/s00795-009-0484-5 PMID: 20683699
58. Milosevic N, Schawalder H, Maier P. Kupffer cell-mediated differential down-regulation of cytochrome P450 metabolism in rat hepatocytes. Eur J Pharmacol 1999; 368:75-87. PMID: 10096772
59. Bataller R, Sancho-Bru P, Gines P, Brenner DA. Liver fibrogenesis: a new role for the renin-angiotensin system. Antioxid Redox Signal 2005; 7:1346-1355. PMID: 16115040
60. Wynn T A, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012; 18:1028-1040. doi: 10.1038/nm.2807 PMID: 22772564
61. DeLeve L D, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 2008; 48:920-930. doi: 10.1002/hep.22351 PMID: 18613151
62. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005; 115:209-218. PMID: 15690074
63. Broering R, Lutterbeck M, Trippler M, Kleinehr K, Poggenpohl L, Paul A, et al. Long-term stimulation of Toll-like receptor 3 in primary human hepatocytes leads to sensitization for antiviral responses induced by poly I:C treatment. J Viral Hepat. 2014; 21: 480-490. doi: 10.1111/jvh.12174 PMID: 24750363