Human skin-derived stem cells as a novel cell source for in vitro hepatotoxicity screening of pharmaceuticals

Stem Cells and Development

Volumn 23, Issue 1, 2014, Pages 44-55

  Rodrigues, Robim M ^a   De Kock, Joery ^a   Branson, Steven ^a   Vinken, Mathieu ^a   Meganathan, Kesavan ^b   Chaudhari, Umesh ^b   Sachinidis, Agapios ^b   Govaere, Olivier ^c   Roskams, Tania ^c   De Boe, Veerle ^d   Vanhaecke, Tamara ^a   Rogiers, Vera ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BIOLOGICAL MARKER; CYTOCHROME P450 1B1; DIMETHYLANILINE MONOOXYGENASE; EPITHELIAL CELL ADHESION MOLECULE; GLUTATHIONE TRANSFERASE A4; GLUTATHIONE TRANSFERASE M3; GROWTH FACTOR; HEME OXYGENASE 1; NERVE CELL ADHESION MOLECULE 2; PARACETAMOL; PROMININ 1; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG; CYTOKINE; SCATTER FACTOR;

ARTICLE; BIOTRANSFORMATION; CELL PROLIFERATION; CHILD; CONTROLLED STUDY; CYTOTOXICITY; DRUG ABSORPTION; DRUG EXPOSURE; DRUG SCREENING; FATTY LIVER; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN SKIN DERIVED STEM CELL; HUMAN TISSUE; IN VITRO STUDY; LIVER CELL; LIVER CELL CULTURE; LIVER INJURY; LIVER NECROSIS; LIVER TOXICITY; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROFESSIONAL KNOWLEDGE; SCHOOL CHILD; STEM CELL; TOXIC HEPATITIS; TOXICOGENETICS; APOPTOSIS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; LIVER; NEURAL CREST; PROCEDURES; SKIN;

APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; DRUG EVALUATION, PRECLINICAL; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; HUMANS; LIVER; NEURAL CREST; SKIN; STEM CELLS;

EID: 84890820918     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0157     Document Type: Article

References (80)

1. Pammolli F, L Magazzini and M Riccaboni. (2011). The productivity crisis in pharmaceutical R&D. Nat Rev Drug Discov 10:428-438.
2. Tamimi NAM and P Ellis. (2009). Drug development: from concept tomarketing. Nephron Clin Pract 113:c125-c131.
3. Schuster D, C Laggner and T Langer. (2005). Why drugs fail-A study on side effects in new chemical entities. Curr Pharm Des 11:3545-3559. (Pubitemid 41300759)
4. Holt MP and C Ju. (2006). Mechanisms of drug-induced liver injury. AAPS J 8:E48-E54.
5. Olson H, G Betton, D Robinson, K Thomas, A Monro, G Kolaja, P Lilly, J Sanders, G Sipes, et al. (2000). Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 32:56-67.
6. Shanks N, R Greek and J Greek. (2009). Are animal models predictive for humans Philos Ethics Humanit Med 4:2.
7. EU. (2006). Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December concerning the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive/45/EC and repealing Council Regulation (EEC) No 793/93 and Commission Regulation (EC) No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/67/EEC, 93/105/EC and 200/21/EC. Off J Eur Union L396:849.
8. EU. (2003). Directive 2003/15/EC of the European Parliament and the Council of 27 February amending Council Directive 76/768/EEC on the approximation of the laws of the Members States relating to cosmetic products. Off J Eur Union L396:849.
9. EU. (2009). Report from the Commission to the Council and the European Parliament-Report on the Development, Validation and Legal Acceptance of Alternative Methods to Animal Tests in the Field of Cosmetics-COM 416 final; http://ec.europa.eu/enterprise/cosmetics/html/cosm animal test.
10. Vanparys P. (2002). ECVAM and pharmaceuticals. Altern Lab Anim 30 Suppl 2:221-223. (Pubitemid 36168742)
11. Guguen-Guillouzo C and A Guillouzo. (2010). General review on in vitro hepatocyte models and their applications. Methods Mol Biol 640:1-40.
12. Schoonen WGEJ, WMA Westerink, JADM de Roos and E Débiton. (2005). Cytotoxic effects of 100 reference compounds on HepG2 and HeLa cells and of 60 compounds on ECC-1 and CHO cells. I mechanistic assays on ROS, glutathione depletion and calcein uptake. Toxicol In Vitro 19:505-516.
13. Jennen DGJ, C Magkoufopoulou, HB Ketelslegers, MHM van Herwijnen, JCS Kleinjans and JHM van Delft. (2010). Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicol Sci 115:66-79.
14. Mills JB, KA Rose, N Sadagopan, J Sahi and SMF de Morais. (2004). Induction of drug metabolism enzymes and MDR1 using a novel human hepatocyte cell line. J Pharmacol Exp Ther 309:303-309. (Pubitemid 38393143)
15. Guillouzo A, A Corlu, C Aninat, D Glaise, F Morel and C Guguen-Guillouzo. (2007). The human hepatoma HepaRG cells: a highly differentiated model for studies of liver metabolismand toxicity of xenobiotics. Chem Biol Interact 168:66-73. (Pubitemid 46659919)
16. LeCluyse EL, RP Witek, ME Andersen and MJ Powers. (2012). Organotypic liver culture models: meeting current challenges in toxicity testing. Crit Rev Toxicol 42:501-548.
17. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147. (Pubitemid 28516247)
18. Takahashi K and S Yamanaka. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676. (Pubitemid 44233629)
19. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49. (Pubitemid 34742565)
20. Jones DL and AJ Wagers. (2008). No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9:11-21.
21. Li L and H Clevers. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327:542-545.
22. Snykers S, T Vanhaecke, P Papeleu, A Luttun, Y Jiang, Y Vander Heyden, C Verfaillie and V Rogiers. (2006). Sequential exposure to cytokines reflecting embryogenesis: the key for in vitro differentiation of adult bone marrow stem cells into functional hepatocyte-like cells. Toxicol Sci 94:330-341; discussion 235. (Pubitemid 44817149)
23. Banas A, T Teratani, Y Yamamoto, M Tokuhara, F Takeshita, G Quinn, H Okochi and T Ochiya. (2007). Adipose tissuederived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46:219-228. (Pubitemid 47171939)
24. Anzalone R, M Lo Iacono, S Corrao, F Magno, T Loria, F Cappello, G Zummo, F Farina and G La Rocca. (2010). New emerging potentials for human Wharton's jelly mesenchymal stem cells: immunological features and hepatocyte-like differentiative capacity. Stem Cells Dev 19:423-438.
25. Tee JY, V Vaghjiani, YH Liu, P Murthi, J Chan and U Manuelpillai. (2013). Immunogenicity and immunomodulatory properties of hepatocyte-like cells derived from human amniotic epithelial cells. Curr Stem Cell Res Ther 8:91-99.
26. Vaghjiani V, V Vaithilingam, B Tuch, W Sievert and U Manuelpillai. (2013). Deriving hepatocyte-like cells from placental cells for transplantation. Curr Stem Cell Res Ther 8:15-24.
27. Toma JG, M Akhavan, KJ Fernandes, F Barnabé-Heider, A Sadikot, DR Kaplan and FD Miller. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784. (Pubitemid 32842682)
28. Biernaskie JA, IA McKenzie, JG Toma and FD Miller. (2006). Isolation of skin-derived precursors (SKPs) and differentiation and enrichment of their Schwann cell progeny. Nat Protoc 1:2803-2812.
29. Jinno H, O Morozova, KL Jones, JA Biernaskie, M Paris, R Hosokawa, MA Rudnicki, Y Chai, F Rossi, MA Marra and FD Miller. (2010). Convergent genesis of an adult neural crest-like dermal stem cell from distinct developmental origins. Stem Cells 28:2027-2040.
30. Gago N, V Pérez-Ló pez, JP Sanz-Jaka, P Cormenzana, I Eizaguirre, A Bernad and A Izeta.(2009). Age-dependent depletion of human skin-derived progenitor cells. Stem Cells 27:1164-1172.
31. Buranasinsup S, M Sila-Asna, N Bunyaratvej and A Bunyaratvej. (2006). In vitro osteogenesis from human skinderived precursor cells. Dev Growth Differ 48:263-269.
32. Hunt DPJ, PN Morris, J Sterling, JA Anderson, A Joannides, C Jahoda, A Compston and S Chandran. (2008). A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26:163-172.
33. Shih DTB, DC Lee, SC Chen, RY Tsai, CT Huang, CC Tsai, EY Shen and WT Chiu. (2005). Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells 23:1012-1020.
34. De Kock J, T Vanhaecke, J Biernaskie, V Rogiers and S Snykers. (2009). Characterization and hepatic differentiation of skin-derived precursors from adult foreskin by sequential exposure to hepatogenic cytokines and growth factors reflecting liver development. Toxicol In Vitro 23:1522-1527.
35. De Kock J, S Snykers, E Ramboer, S Demeester, A Heymans, S Branson, T Vanhaecke and V Rogiers. (2011). Evaluation of the multipotent character of human foreskin-derived precursor cells. Toxicol In Vitro 25:1191-1202.
36. De Kock J, M Najar, J Bolleyn, F Al Battah, RM Rodrigues, K Buyl, G Raicevic, O Govaere, S Branson, et al. (2012). Mesoderm-derived stem cells: the link between the transcriptome and their differentiation potential. Stem Cells Dev 21:3309-3323.
37. James LP, PR Mayeux and JA Hinson. (2003). Acetaminophen-induced hepatotoxicity. Drug Metab Dispos 31:1499-1506. (Pubitemid 37466918)
38. McGill MR, MR Sharpe, CD Williams, M Taha, SC Curry and H Jaeschk. (2012). The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation. J Clin Invest 122:1574-1583.
39. Zimmerman HJ and WC Maddrey. (1995). Acetaminophen (paracetamol) hepatotoxicity with regular intake of alcohol: analysis of instances of therapeutic misadventure. Hepatology 22:767-773.
40. Mosmann T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63. (Pubitemid 14203433)
41. Urushidani T. (2005). Toxicogenomics: Japanese initiative. In: Handbook of Toxicogenomics. Borlak J. Wiley GmbH Co KGaA, Weinheim, Germany, pp. 623-631.
42. Uehara T, A Ono, T Maruyama, I Kato, H Yamada, Y Ohno and T Urushidani. (2010). The Japanese toxicogenomics project: application of toxicogenomics. Mol Nutr Food Res 54:218-227.
43. Irizarry RA, BM Bolstad, F Collin, LM Cope, B Hobbs and TP Speed. (2003). Summaries of affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15.
44. Verma S and N Kaplowitz. (2009). Diagnosis, management and prevention of drug-induced liver injury. Gut 58:1555-1564.
45. Guillouzo A. (1998). Liver cell models in in vitro toxicology. Environ Health Perspect 106 Suppl 2:511-532. (Pubitemid 28256760)
46. Ilic D and JM Polak. (2011). Stem cells in regenerative medicine: introduction. Br Med Bull 98:117-126.
47. Joery DK, MR Robim, B Jennifer, V Tamara and R Vera. (2012). Focus on stem cells as sources of human target cell for in vitro research and testing. ALTEX 29:3-10.
48. Schmelzer E, E Wauthier and LM Reid. (2006). The phenotypes of pluripotent human hepatic progenitors. Stem Cells 24:1852-1858. (Pubitemid 44474161)
49. Yoon SM, D Gerasimidou, R Kuwahara, P Hytiroglou, JE Yoo, YN Park and ND Theise. (2011). Epithelial cell adhesion molecule (EpCAM) marks hepatocytes newly derived from stem/progenitor cells in humans. Hepatology 53:964-973.
50. Zhou H. (2007). Identification of hepatocytic and bile ductular cell lineages and candidate stem cells in bipolar ductular reactions in cirrhotic human liver. Hepatology 45:716-724. (Pubitemid 46450623)
51. Crosby HA, DA Kelly and AJ Strain. (2001). Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium. Gastroenterology 120:534-544. (Pubitemid 32147651)
52. Mishra L, T Banker, J Murray, S Byers, A Thenappan, AR He, K Shetty, L Johnson and EP Reddy. (2009). Liver stem cells and hepatocellular carcinoma. Hepatology 49:318-329.
53. Kitisin K, N Ganesan, Y Tang, W Jogunoori, EA Volpe, SS Kim, V Katuri, B Kallakury, M Pishvaian, et al. (2007). Disruption of transforming growth factor-beta signaling through beta-spectrin ELF leads to hepatocellular cancer through cyclin D1 activation. Oncogene 26:7103-7110. (Pubitemid 350059676)
54. Herrera MB, S Bruno, S Buttiglieri, C Tetta, S Gatti, MC Deregibus, B Bussolati and G Camussi. (2006). Isolation and characterization of a stem cell population from adult human liver. Stem Cells 24:2840-2850. (Pubitemid 46053020)
55. Seki E and DA Brenner. (2008). Toll-like receptors and adaptor molecules in liver disease: update. Hepatology 48: 322-335. (Pubitemid 351975556)
56. Takeda K and S Akira. (2000). STAT family of transcription factors in cytokine-mediated biological responses. Cytokine Growth Factor Rev 11:199-207. (Pubitemid 30337459)
57. Zhao R, AJ Watt, J Li, J Luebke-Wheeler, EE Morrisey and SA Duncan. (2005). GATA6 is essential for embryonic development of the liver but dispensable for early heart formation. Mol Cell Biol 25:2622-2631. (Pubitemid 40381626)
58. Sirois J, J-F Cote, A Charest, N Uetani, A Bourdeau, SA Duncan, E Daniels and ML Tremblay. (2006). Essential function of PTP-PEST during mouse embryonic vascularization, mesenchyme formation, neurogenesis and early liver development. Mech Dev 123:869-880. (Pubitemid 44829933)
59. Nukaya M, JA Walisser, SM Moran, GD Kennedy and CA Bradfield. (2010). Aryl hydrocarbon receptor nuclear translocator in hepatocytes is required for aryl hydrocarbon receptor-mediated adaptive and toxic responses in liver. Toxicol Sci 118:554-563.
60. Klaassen CD and LM Aleksunes. (2010). Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol Rev 62:1-96.
61. Rand EB, AM Depaoli, NO Davidson, GI Bell and CF Burant. (1993). Sequence, tissue distribution, and functional characterization of the rat fructose transporter GLUT5. Am J Physiol 264:G1169-G1176. (Pubitemid 23196823)
62. Larson AM, J Polson, RJ Fontana, TJ Davern, E Lalani, LS Hynan, JS Reisch, FV Schiødt, G Ostapowicz, et al. (2005). Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 42:1364-1372. (Pubitemid 43260039)
63. Scott DJ, AS Devonshire, YA Adeleye, ME Schutte, MR Rodrigues, TM Wilkes, MG Sacco, L Gribaldo, M Fabbri, et al. (2011). Inter-and intra-laboratory study to determine the reproducibility of toxicogenomics datasets. Toxicology 290:50-58.
64. Cheng F, D Theodorescu, IG Schulman and JK Lee. (2011). In vitro transcriptomic prediction of hepatotoxicity for early drug discovery. J Theor Biol 290:27-36.
65. Hirode M, A Ono, T Miyagishima, T Nagao, Y Ohno and T Urushidani. (2008). Gene expression profiling in rat liver treated with compounds inducing phospholipidosis. Toxicol Appl Pharmacol 229:290-299.
66. Hirode M, A Horinouchi, T Uehara, A Ono, T Miyagishima, H Yamada, T Nagao, Y Ohno and T Urushidani. (2009). Gene expression profiling in rat liver treated with compounds inducing elevation of bilirubin. Hum Exp Toxicol 28:231-244.
67. HirodeM, K Omura, N Kiyosawa, T Uehara, T Shimuzu, A Ono, T Miyagishima, T Nagao, Y Ohno and T Urushidani. (2009). Gene expression profiling in rat liver treated with various hepatotoxic-compounds inducing coagulopathy. J Toxicol Sci 34:281-293.
68. Uehara T, M Hirode, A Ono, N Kiyosawa, K Omura, T Shimizu, Y Mizukawa, T Miyagishima, T Nagao and T Urushidani (2008). A toxicogenomics approach for early assessment of potential non-genotoxic hepatocarcinogenicity of chemicals in rats. Toxicology 250:15-26.
69. Uehara T, N Kiyosawa, M Hirode, K Omura, T Shimizu, A Ono, Y Mizukawa, T Miyagishima, T Nagao and T Urushidani. (2008). Gene expression profiling of methapyrileneinduced hepatotoxicity in rat. J Toxicol Sci 33:37-50. (Pubitemid 351340762)
70. Blomme EAG, Y Yang and JF Waring. (2009). Use of toxicogenomics to understand mechanisms of drug-induced hepatotoxicity during drug discovery and development. Toxicol Lett 186:22-31.
71. Foster WR, SJ Chen, A He, A Truong, V Bhaskaran, DM Nelson, DM Dambach, LD Lehman-McKeeman and BD Car. (2007). A retrospective analysis of toxicogenomics in the safety assessment of drug candidates. Toxicol Pathol 35:621-635. (Pubitemid 47123742)
72. O'Connor L, A Strasser, LA O'Reilly, G Hausmann, JM Adams, S Cory and DC Huang. (1998). Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J 17:384-395. (Pubitemid 28045479)
73. Yang JY, W Xia and MCT Hu. (2006). Ionizing radiation activates expression of FOXO3a, Fas ligand, and Bim, and induces cell apoptosis. Int J Oncol 29:643-648.
74. Sarma SN, Y-J Kim, M Song and J-C Ryu. (2011). Induction of apoptosis in human leukemia cells through the production of reactive oxygen species and activation of HMOX1 and Noxa by benzene, toluene, and o-xylene. Toxicology 280:109-117.
75. Wagner EF. (2002). Functions of AP1 (Fos/Jun) in bone development. Ann Rheum Dis 61 Suppl 2:ii40-ii42. (Pubitemid 35221711)
76. Kallio JP, S Hopkins-Donaldson, AH Baker and VM Kähä ri. (2011). TIMP-3 promotes apoptosis in nonadherent small cell lung carcinoma cells lacking functional death receptor pathway. Int J Cancer 128:991-996.
77. Nebert DW, TP Dalton, AB Okey and FJ Gonzalez. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279:23847-23850. (Pubitemid 38725238)
78. Thiele K, T Kessler, P Arck, A Erhardt and G Tiegs. (2013). Acetaminophen and pregnancy: short-and long-term consequences for mother and child. J Reprod Immunol 97:128-139.
79. Ring JA, H Ghabrial, MS Ching, RA Smallwood and DJ Morgan. (1999). Fetal hepatic drug elimination. Pharmacol Ther 84:429-445.
80. Gow PJ, H Ghabrial, RA Smallwood, DJ Morgan and MS Ching. (2001). Neonatal hepatic drug elimination. Pharmacol Toxicol 88:3-15. (Pubitemid 32113216)