Pluripotent stem cell-derived hepatocyte-like cells.

Liver disease is an important clinical problem, impacting over 30 million Americans and over 600 million people worldwide. It is the 12th leading cause of death in the United States and the 16th worldwide. Due to a paucity of donor organs, several thousand Americans die yearly while waiting for liver transplantation. Unfortunately, alternative tissue sources such as fetal hepatocytes and hepatic cell lines are unreliable, difficult to reproduce, and do not fully recapitulate hepatocyte phenotype and functions. As a consequence, alternative cell sources that do not have these limitations have been sought. Human embryonic stem (hES) cell- and induced pluripotent stem (iPS) cell-derived hepatocyte-like cells may enable cell based therapeutics, the study of the mechanisms of human disease and human development, and provide a platform for screening the efficacy and toxicity of pharmaceuticals. iPS cells can be differentiated in a step-wise fashion with high efficiency and reproducibility into hepatocyte-like cells that exhibit morphologic and phenotypic characteristics of hepatocytes. In addition, iPS-derived hepatocyte-like cells (iHLCs) possess some functional hepatic activity as they secrete urea, alpha-1-antitrypsin, and albumin. However, the combined phenotypic and functional traits exhibited by iHLCs resemble a relatively immature hepatic phenotype that more closely resembles that of fetal hepatocytes rather than adult hepatocytes. Specifically, iHLCs express fetal markers such as alpha-fetoprotein and lack key mature hepatocyte functions, as reflected by drastically reduced activity (~0.1%) of important detoxification enzymes (i.e. CYP2A6, CYP3A4). These key differences between iHLCs and primary adult human hepatocytes have limited the use of stem cells as a renewable source of functional adult hepatocytes for in vitro and in vivo applications. Unfortunately, the developmental pathways that control hepatocyte maturation from a fetal into an adult hepatocyte are poorly understood, which has hampered the field in its efforts to induce further maturation of iPS-derived hepatic lineage cells. This review analyzes recent developments in the derivation of hepatocyte-like cells, and proposes important points to consider and assays to perform during their characterization. In the future, we envision that iHLCs will be used as in vitro models of human disease, and in the longer term, provide an alternative cell source for drug testing and clinical therapy.

[1]  S. Bhatia,et al.  An extracellular matrix microarray for probing cellular differentiation , 2005, Nature Methods.

[2]  J. Rossant,et al.  Liver Organogenesis Promoted by Endothelial Cells Prior to Vascular Function , 2001, Science.

[3]  K. Audus,et al.  Formation of extensive canalicular networks by rat hepatocytes cultured in collagen-sandwich configuration. , 1994, The American journal of physiology.

[4]  J Spizek,et al.  Biotechnology advances. , 1990, Biotechnology advances.

[5]  T. Starzl,et al.  Orthotopic homotransplantation of the human liver. , 1968 .

[6]  Yvonne Will,et al.  Use of micropatterned cocultures to detect compounds that cause drug-induced liver injury in humans. , 2013, Toxicological sciences : an official journal of the Society of Toxicology.

[7]  P. Bosma,et al.  Long-term amelioration of bilirubin glucuronidation defect in Gunn rats by transplanting genetically modified immortalized autologous hepatocytes. , 1998, Cell transplantation.

[8]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[9]  Sylvia Stracke,et al.  Genome-Wide Association and Functional Follow-Up Reveals New Loci for Kidney Function , 2012, PLoS genetics.

[10]  M. Sakaguchi,et al.  Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. , 2000, Science.

[11]  A. Nussler,et al.  In Vitro Differentiated Adult Human Liver Progenitor Cells Display Mature Hepatic Metabolic Functions: A Potential Tool for in Vitro Pharmacotoxicological Testing , 2011, Cell transplantation.

[12]  T. Starzl,et al.  Themes of liver transplantation , 2010, Hepatology.

[13]  J. White,et al.  Evaluation of a hepatocyte‐entrapment hollow fiber bioreactor: A potential bioartificial liver , 1993, Biotechnology and bioengineering.

[14]  S. Strom,et al.  Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. , 1998, The New England journal of medicine.

[15]  M. Elazar,et al.  Isolation and Transcriptional Profiling of Purified Hepatic Cells Derived from Human Embryonic Stem Cells , 2008, Stem cells.

[16]  Junji Fukuda,et al.  Novel hepatocyte culture system developed using microfabrication and collagen/polyethylene glycol microcontact printing. , 2006, Biomaterials.

[17]  J. Ott,et al.  Family-based designs for genome-wide association studies , 2011, Nature Reviews Genetics.

[18]  Liang-Shang Gan,et al.  Effects of prototypical microsomal enzyme inducers on cytochrome P450 expression in cultured human hepatocytes. , 2003, Drug metabolism and disposition: the biological fate of chemicals.

[19]  Takanori Takebe,et al.  Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant , 2014, Nature Protocols.

[20]  李亚明,et al.  Hepatocyte transplantation , 2005 .

[21]  M. Weiss,et al.  Self-renewing endodermal progenitor lines generated from human pluripotent stem cells. , 2012, Cell stem cell.

[22]  Masahiro Ito,et al.  Review of hepatocyte transplantation. , 2009, Journal of hepato-biliary-pancreatic surgery.

[23]  G. Michalopoulos,et al.  Liver Regeneration , 1997, Journal of cellular physiology.

[24]  Ludovic Vallier,et al.  Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. , 2010, The Journal of clinical investigation.

[25]  K. Zaret,et al.  A bipotential precursor population for pancreas and liver within the embryonic endoderm. , 2001, Development.

[26]  Stephen Dalton,et al.  Highly efficient generation of human hepatocyte–like cells from induced pluripotent stem cells , 2010, Hepatology.

[27]  Cécile Legallais,et al.  A cocktail of metabolic probes demonstrates the relevance of primary human hepatocyte cultures in a microfluidic biochip for pharmaceutical drug screening. , 2011, International journal of pharmaceutics.

[28]  Peter V. Henstock,et al.  Cellular imaging predictions of clinical drug-induced liver injury. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[29]  Sangeeta N Bhatia,et al.  Modeling hepatitis C virus infection using human induced pluripotent stem cells , 2012, Proceedings of the National Academy of Sciences.

[30]  Aarati R. Ranade,et al.  Robust expansion of human hepatocytes in Fah−/−/Rag2−/−/Il2rg−/− mice , 2007, Nature Biotechnology.

[31]  David M. Gilbert,et al.  Productive Hepatitis C Virus Infection of Stem Cell-Derived Hepatocytes Reveals a Critical Transition to Viral Permissiveness during Differentiation , 2012, PLoS pathogens.

[32]  S. Strom,et al.  Human hepatocyte transplantation. , 2010, Methods in molecular biology.

[33]  Sangeeta N. Bhatia,et al.  Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures , 2010, Proceedings of the National Academy of Sciences.

[34]  E. Kroon,et al.  Efficient differentiation of human embryonic stem cells to definitive endoderm , 2005, Nature Biotechnology.

[35]  S. Caritis,et al.  A sensitive and specific CYP cocktail assay for the simultaneous assessment of human cytochrome P450 activities in primary cultures of human hepatocytes using LC-MS/MS. , 2013, Journal of pharmaceutical and biomedical analysis.

[36]  Sayaka Sekiya,et al.  Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors , 2011, Nature.

[37]  Susan Lindquist,et al.  Generation of Isogenic Pluripotent Stem Cells Differing Exclusively at Two Early Onset Parkinson Point Mutations , 2011, Cell.

[38]  M L Yarmush,et al.  Effect of cell–cell interactions in preservation of cellular phenotype: cocultivation of hepatocytes and nonparenchymal cells , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[39]  S. Bhatia,et al.  Microenvironmental regulation of the sinusoidal endothelial cell phenotype in vitro , 2009, Hepatology.

[40]  R. Deo,et al.  The zebrafish:scalable in vivo modeling for systems biology , 2011, Wiley interdisciplinary reviews. Systems biology and medicine.

[41]  C. Guillemette,et al.  Three-dimensional culture and cAMP signaling promote the maturation of human pluripotent stem cell-derived hepatocytes , 2013, Development.

[42]  Neta Lavon Generation of hepatocytes from human embryonic stem cells. , 2010, Methods in molecular biology.

[43]  S. Nyberg,et al.  Cell therapies for liver diseases , 2012, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[44]  Deborah A Nickerson,et al.  Genome-wide studies of copy number variation and exome sequencing identify rare variants in BAG3 as a cause of dilated cardiomyopathy. , 2011, American journal of human genetics.

[45]  Anne E Carpenter,et al.  A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. , 2013, Cell host & microbe.

[46]  M. Yarmush,et al.  Enrichment of hepatocyte-like cells with upregulated metabolic and differentiated function derived from embryonic stem cells using S-NitrosoAcetylPenicillamine. , 2009, Tissue engineering. Part C, Methods.

[47]  E. Simpson,et al.  Modelling Human Regulatory Variation in Mouse: Finding the Function in Genome-Wide Association Studies and Whole-Genome Sequencing , 2012, PLoS genetics.

[48]  M. Grompe,et al.  Generation and Regeneration of Cells of the Liver and Pancreas , 2008, Science.

[49]  J. Roy-Chowdhury,et al.  Hepatocyte transplantation , 2004, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[50]  A. Daly Using genome-wide association studies to identify genes important in serious adverse drug reactions. , 2012, Annual review of pharmacology and toxicology.

[51]  A. Guillouzo,et al.  Liver cell models in in vitro toxicology. , 1998, Environmental health perspectives.

[52]  L. Marchionni,et al.  In Vivo Liver Regeneration Potential of Human Induced Pluripotent Stem Cells from Diverse Origins , 2011, Science Translational Medicine.

[53]  Anne E Carpenter,et al.  Identification of small molecules for human hepatocyte expansion and iPS differentiation , 2013, Nature chemical biology.

[54]  Toshiaki Maruyama,et al.  Complete Replication of Hepatitis C Virus in Cell Culture , 2005, Science.

[55]  Luvena L. Ong,et al.  Humanized mice with ectopic artificial liver tissues , 2011, Proceedings of the National Academy of Sciences.

[56]  S. Yamanaka,et al.  Induced pluripotent stem cell-derived hepatocytes have the functional and proliferative capabilities needed for liver regeneration in mice. , 2010, The Journal of clinical investigation.

[57]  P. Souček,et al.  Different in vitro metabolism of paclitaxel and docetaxel in humans, rats, pigs, and minipigs. , 2004, Drug metabolism and disposition: the biological fate of chemicals.

[58]  E L LeCluyse,et al.  Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. , 2001, European journal of pharmaceutical sciences : official journal of the European Federation for Pharmaceutical Sciences.

[59]  D. Hay,et al.  Progress and future challenges in stem cell-derived liver technologies. , 2009, American journal of physiology. Gastrointestinal and liver physiology.

[60]  E. Keeffe,et al.  Chronic viral hepatitis: epidemiology, molecular biology, and antiviral therapy. , 2011, Frontiers in bioscience.

[61]  M. Zilliox,et al.  Efficient assembly of rat hepatocyte spheroids for tissue engineering applications , 1996, Biotechnology and bioengineering.

[62]  A. Schambach,et al.  Rescue of ATP7B function in hepatocyte-like cells from Wilson's disease induced pluripotent stem cells using gene therapy or the chaperone drug curcumin. , 2011, Human molecular genetics.

[63]  C. Rogler,et al.  Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus , 2001, Hepatology.

[64]  M. Perera,et al.  Liver transplantation: Issues for the next 20 years , 2009, Journal of gastroenterology and hepatology.

[65]  J. Maher,et al.  Support of cultured hepatocytes by a laminin-rich gel. Evidence for a functionally significant subendothelial matrix in normal rat liver. , 1987, The Journal of clinical investigation.

[66]  K. Tilmant,et al.  Characterization of primary human hepatocytes, HepG2 cells, and HepaRG cells at the mRNA level and CYP activity in response to inducers and their predictivity for the detection of human hepatotoxins , 2012, Cell Biology and Toxicology.

[67]  Catherine Payne,et al.  Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling , 2008, Proceedings of the National Academy of Sciences.

[68]  R. Tompkins,et al.  Hepatocyte function and extracellular matrix geometry: long‐term culture in a sandwich configuration , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[69]  M. Yarmush,et al.  Amino acid‐mediated heterotypic interaction governs performance of a hepatic tissue model , 2009, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[70]  P. Currie,et al.  Animal models of human disease: zebrafish swim into view , 2007, Nature Reviews Genetics.

[71]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[72]  Brian S. Clark,et al.  JD induced pluripotent stem cell–derived hepatocytes faithfully recapitulate the pathophysiology of familial hypercholesterolemia , 2012, Hepatology.

[73]  Sangeeta N Bhatia,et al.  Assessing porcine liver-derived biomatrix for hepatic tissue engineering. , 2004, Tissue engineering.

[74]  P. Zandstra,et al.  Reproducible, Ultra High-Throughput Formation of Multicellular Organization from Single Cell Suspension-Derived Human Embryonic Stem Cell Aggregates , 2008, PloS one.

[75]  Frank Stahl,et al.  Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties. , 2003, Drug metabolism and disposition: the biological fate of chemicals.

[76]  A. Wolkoff,et al.  Heterogeneous accumulation of fluorescent bile acids in primary rat hepatocytes does not correlate with their homogenous expression of ntcp. , 2011, American journal of physiology. Gastrointestinal and liver physiology.

[77]  J. Castell,et al.  Hepatocyte cell lines: their use, scope and limitations in drug metabolism studies , 2006, Expert opinion on drug metabolism & toxicology.

[78]  I. Kola,et al.  Can the pharmaceutical industry reduce attrition rates? , 2004, Nature Reviews Drug Discovery.

[79]  Xiaolei Yin,et al.  Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells , 2009, Cell Research.

[80]  R. Pedersen,et al.  Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development , 2010, Hepatology.

[81]  Robert Hoehndorf,et al.  Mouse genetic and phenotypic resources for human genetics , 2012, Human mutation.

[82]  M. Toner,et al.  Microengineering of cellular interactions. , 2000, Annual review of biomedical engineering.

[83]  E. Novik,et al.  Prediction of human hepatic clearance using an in vitro plated hepatocyte clearance model. , 2009, Drug metabolism letters.

[84]  K. Zaret,et al.  Dynamic Signaling Network for the Specification of Embryonic Pancreas and Liver Progenitors , 2009, Science.

[85]  D. Jaeck,et al.  Comparison of the stability of some major cytochrome P450 and conjugation reactions in rat, dog and human hepatocyte monolayers , 2010, European Journal of Drug Metabolism and Pharmacokinetics.

[86]  Wei-Shou Hu,et al.  Enhanced Cytochrome P450 IA1 Activity of Self-Assembled Rat Hepatocyte Spheroids , 1999, Cell transplantation.

[87]  Takanori Takebe,et al.  Vascularized and functional human liver from an iPSC-derived organ bud transplant , 2013, Nature.

[88]  M. Toner,et al.  Enhanced differentiation of embryonic stem cells using co‐cultivation with hepatocytes , 2008, Biotechnology and bioengineering.

[89]  J. Roy-Chowdhury,et al.  Hepatocyte transplantation. , 2004, Journal of hepatology.

[90]  Jonathan L. Linehan,et al.  Defined conditions for development of functional hepatic cells from human embryonic stem cells. , 2005, Stem cells and development.

[91]  R. Bartenschlager,et al.  Production of infectious hepatitis C virus in tissue culture from a cloned viral genome , 2005, Nature Medicine.

[92]  Alejandro Soto-Gutiérrez,et al.  Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. , 2009, Gastroenterology.

[93]  D. B. Duignan,et al.  Assessment of a Micropatterned Hepatocyte Coculture System to Generate Major Human Excretory and Circulating Drug Metabolites , 2010, Drug Metabolism and Disposition.

[94]  Hongbin Yu,et al.  Special Section on Prediction of Human Pharmacokinetic Parameters from In Vitro Systems Meeting the Challenge of Predicting Hepatic Clearance of Compounds Slowly Metabolized by Cytochrome P450 Using a Novel Hepatocyte Model, HepatoPac , 2013 .

[95]  B. Thiers Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors , 2008 .

[96]  L. Hui,et al.  Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors , 2011, Nature.