Microbial-Derived Lithocholic Acid and Vitamin K2 Drive the Metabolic Maturation of Pluripotent Stem Cells-Derived and Fetal Hepatocytes

Hepatology

Volumn 62, Issue 1, 2015, Pages 265-278

  Avior, Yishai ^a   Levy, Gahl ^a   Zimerman, Michal ^a   Kitsberg, Daniel ^a   Schwartz, Robert ^b   Sadeh, Ronen ^a   Moussaieff, Arieh ^a   Cohen, Merav ^a   Itskovitz Eldor, Joseph ^c   Nahmias, Yaakov ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ALPHA 1 ANTITRYPSIN; APOLIPOPROTEIN B100; ARGINASE; ARGININOSUCCINATE SYNTHASE; AROMATIC HYDROCARBON RECEPTOR; ASIALOGLYCOPROTEIN RECEPTOR; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1A2; CYTOCHROME P450 2C9; CYTOCHROME P450 2D6; CYTOCHROME P450 3A4; CYTOCHROME P450 3A7; FARNESOID X RECEPTOR; FARNOQUINONE; FIBROBLAST GROWTH FACTOR 2; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; LITHOCHOLIC ACID; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 1; OCTAMER TRANSCRIPTION FACTOR 4; OMEPRAZOLE; PREGNANE X RECEPTOR; RIFAMPICIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR SOX2; CYTOCHROME P450 3A; MENATETRENONE; STEROID RECEPTOR;

ACUTE TOXICITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CHOLESTASIS; CONTROLLED STUDY; DRUG METABOLISM; FATTY LIVER; FETUS LIVER; FLOW CYTOMETRY; HEPG2 CELL LINE; HUMAN; HUMAN TISSUE; INTESTINE FLORA; LIVER CELL; LIVER TOXICITY; PLURIPOTENT STEM CELL; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCREENING TEST; TC50; TOXIC CONCENTRATION; TOXICOLOGY; TRANSIENT EXPRESSION; ANALOGS AND DERIVATIVES; CELL CULTURE; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; EMBRYONIC STEM CELL; ENZYMOLOGY; METABOLISM; SEQUENCE ANALYSIS; TOXICITY TESTING;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOCHROME P-450 CYP2C9; CYTOCHROME P-450 CYP3A; EMBRYONIC STEM CELLS; HEPATOCYTES; HUMANS; LITHOCHOLIC ACID; PLURIPOTENT STEM CELLS; RECEPTORS, STEROID; SEQUENCE ANALYSIS, RNA; TOXICITY TESTS, ACUTE; VITAMIN K 2;

EID: 84933181542     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27803     Document Type: Article

References (42)

1. Guengerich FP. Cytochrome P450 and chemical toxicology. Chem Res Toxicol 2007;21:70-83.
2. Kaplowitz N. Idiosyncratic drug hepatotoxicity. Nat Rev Drug Discov 2005;4:489-499.
3. Gottmann E, Kramer S, Pfahringer B, Helma C. Data quality in predictive toxicology: reproducibility of rodent carcinogenicity experiments. Environ Health Perspect 2001;109:509-514.
4. Olson H, Betton G, Robinson D, Thomas K, Monro A, Kolaja G, et al. Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 2000;32:56-67.
5. LeCluyse EL. Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. Eur J Pharm Sci 2001;13:343-368.
6. Guillouzo A. Liver cell models in in vitro toxicology. Environ Health Perspect 1998;106(Suppl 2):511-532.
7. Hewitt NJ, Lechon MJ, Houston JB, Hallifax D, Brown HS, Maurel P, et al. Primary hepatocytes: current understanding of the regulation of metabolic enzymes and transporter proteins, and pharmaceutical practice for the use of hepatocytes in metabolism, enzyme induction, transporter, clearance, and hepatotoxicity studies. Drug Metab Rev 2007;39:159-234.
8. Nahmias Y, Berthiaume F, Yarmush ML. Integration of technologies for hepatic tissue engineering. Adv Biochem Eng Biotechnol 2007;103:309-329.
9. Kidambi S, Yarmush RS, Novik E, Chao P, Yarmush ML, Nahmias Y. Oxygen-mediated enhancement of primary hepatocyte metabolism, functional polarization, gene expression, and drug clearance. Proc Natl Acad Sci U S A 2009;106:15714-15719.
10. Khetani SR, Bhatia SN. Microscale culture of human liver cells for drug development. Nat Biotechnol 2008;26:120-126.
11. Shulman M, Nahmias Y. Long-term culture and coculture of primary rat and human hepatocytes. Methods Mol Biol 2013;945:287-302.
12. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 2002;109:1291-1302.
13. Stock P, Bruckner S, Ebensing S, Hempel M, Dollinger MM, Christ B. The generation of hepatocytes from mesenchymal stem cells and engraftment into murine liver. Nat Protoc 2010;5:617-627.
14. Lue J, Lin G, Ning H, Xiong A, Lin CS, Glenn JS. Transdifferentiation of adipose-derived stem cells into hepatocytes: a new approach. Liver Int 2010;30:913-922.
15. Zhu S, Rezvani M, Harbell J, Mattis AN, Wolfe AR, Benet LZ, et al. Mouse liver repopulation with hepatocytes generated from human fibroblasts. Nature 2014;508:93-97.
16. Duan Y, Ma X, Zou W, Wang C, Bahbahan IS, Ahuja TP, et al. Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells 2010;28:674-686.
17. Song Z, Cai J, Liu Y, Zhao D, Yong J, Duo S, et al. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 2009;19:1233-1242.
18. Si-Tayeb K, Noto FK, Nagaoka M, Li J, Battle MA, Duris C, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010;51:297-305.
19. Chen YF, Tseng CY, Wang HW, Kuo HC, Yang VW, Lee OK. Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology 2012;55:1193-1203.
20. Roelandt P, Vanhove J, Verfaillie C. Directed differentiation of pluripotent stem cells to functional hepatocytes. Methods Mol Biol 2013;997:141-147.
21. Szkolnicka D, Farnworth SL, Lucendo-Villarin B, Storck C, Zhou W, Iredale JP, et al. Accurate prediction of drug-induced liver injury using stem cell-derived populations. Stem Cells Transl Medicine 2014;3:141-148.
22. 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.
23. Morelli L. Postnatal development of intestinal microflora as influenced by infant nutrition. J Nutr 2008;138:1791S-1795S.
24. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, et al. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci U S A 2001;98:3369-3374.
25. Conly JM, Stein K. The production of menaquinones (vitamin K2) by intestinal bacteria and their role in maintaining coagulation homeostasis. Prog Food Nutr Sci 1992;16:307-343.
26. Shearer MJ, Rahim S, Barkhan P, Stimmler L. Plasma vitamin K1 in mothers and their newborn babies. Lancet 1982;2:460-463.
27. Shearer MJ. Vitamin K deficiency bleeding (VKDB) in early infancy. Blood Rev 2009;23:49-59.
28. Tabb MM, Sun A, Zhou C, Grun F, Errandi J, Romero K, et al. Vitamin K2 regulation of bone homeostasis is mediated by the steroid and xenobiotic receptor SXR. J Biol Chem 2003;278:43919-43927.
29. Ichikawa T, Horie-Inoue K, Ikeda K, Blumberg B, Inoue S. Steroid and xenobiotic receptor SXR mediates vitamin K2-activated transcription of extracellular matrix-related genes and collagen accumulation in osteoblastic cells. J Biol Chem 2006;281:16927-16934.
30. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000;227:271-278.
31. Amit M, Chebath J, Margulets V, Laevsky I, Miropolsky Y, Shariki K, et al. Suspension culture of undifferentiated human embryonic and induced pluripotent stem cells. Stem Cell Rev 2010;6:248-259.
32. Goodwin B, Hodgson E, Liddle C. The orphan human pregnane X receptor mediates the transcriptional activation of CYP3A4 by Rifampicin through a distal enhancer module. Mol Pharmacol 1999;56:1329-1339.
33. Goldwasser J, Cohen PY, Lin W, Kitsberg D, Balaguer P, Polyak SJ, et al. Naringenin inhibits the assembly and long-term production of infectious hepatitis C virus particles through a PPAR-mediated mechanism. J Hepatol 2011;55:963-971.
34. Behnia K, Bhatia S, Jastromb N, Balis U, Sullivan S, Yarmush M, Toner M. Xenobiotic metabolism by cultured primary porcine hepatocytes. Tissue Eng 2000;6:467-479.
35. Donato MT, Jimenez N, Castell JV, Gomez-Lechon MJ. Fluorescence-based assays for screening nine cytochrome P450 (P450) activities in intact cells expressing individual human P450 enzymes. Drug Metab Dispos 2004;32:699-706.
36. Kamiya A, Kinoshita T, Miyajima A. Oncostatin M and hepatocyte growth factor induce hepatic maturation via distinct signaling pathways. FEBS Lett 2001;492:90-94.
37. Mooiman KD, Maas-Bakker RF, Moret EE, Beijnen JH, Schellens JH, Meijerman I. Milk thistle's active components silybin and isosilybin: novel inhibitors of PXR-mediated CYP3A4 induction. Drug Metab Dispos 2013;41:1494-1504.
38. Roelandt P, Obeid S, Paeshuyse J, Vanhove J, Van Lommel A, Nahmias Y, et al. Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus. J Hepatol 2012;57:246-251.
39. Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 2013;499:481-484.
40. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, et al. Identification of a nuclear receptor for bile acids. Science 1999;284:1362-1365.
41. Gronlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999;28:19-25.
42. Hopkins MJ, Macfarlane GT, Furrie E, Fite A, Macfarlane S. Characterisation of intestinal bacteria in infant stools using real-time PCR and northern hybridisation analyses. FEMS Microbiol Ecol 2005;54:77-85.