From Human-Induced Pluripotent Stem Cells to Liver Disease Modeling: A Focus on Dyslipidemia

Current Pathobiology Reports

Volumn 3, Issue 1, 2015, Pages 47-56

  Idriss, Salam ^a,b,c,e   Zibara, Kazem ^c   Cariou, Bertrand ^a,b,d,e   Si Tayeb, Karim ^a,b,e  

^a L INSTITUT DU THORAX   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c LEBANESE UNIVERSITY   (Lebanon)

^d NANTES UNIVERSITY HOSPITAL   (France)

^e NONE   (France)

Author keywords

Differentiation; Hepatocytes; hiPSCs; Hypercholesterolemia; Liver development; Metabolic disease

Indexed keywords

EID: 85019299966     PISSN: None     EISSN: 2167485X     Source Type: Journal    
DOI: 10.1007/s40139-015-0067-1     Document Type: Review

References (89)

1. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676. doi:10.1016/j.cell.2006.07.024
2. Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872. doi:10.1016/j.cell.2007.11.019
3. Yu J, Vodyanik MA, Smuga-Otto K et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920. doi:10.1126/science.1151526
4. Yamanaka S (2012) Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10(6):678–684. doi:10.1016/j.stem.2012.05.005
5. Nordin N, Lai MI, Veerakumarasivam A, Ramasamy R (2011) Induced pluripotent stem cells: history, properties and potential applications. Med J Malaysia 66(1):4–9
6. Park I-H, Zhao R, West JA et al (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451(7175):141–146. doi:10.1038/nature06534
7. Robinton D, Daley G (2012) The promise of induced pluripotent stem cells in research and therapy. Nature 481(7381):295–305. doi:10.1038/nature10761
8. Wernig M, Meissner A, Foreman R et al (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448(7151):318–324. doi:10.1038/nature05944
9. Hockemeyer D, Soldner F, Cook EG, Gao Q, Mitalipova M, Jaenisch R (2008) A drug-inducible system for direct reprogramming of human somatic cells to pluripotency. Cell Stem Cell 3(3):346–353. doi:10.1016/j.stem.2008.08.014
10. Maherali N, Ahfeldt T, Rigamonti A, Utikal J, Cowan C, Hochedlinger K (2008) A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 3(3):340–345. doi:10.1016/j.stem.2008.08.003
11. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27(3):275–280. doi:10.1038/nbt.1529
12. Dimos JT, Rodolfa KT, Niakan KK et al (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321(5893):1218–1221. doi:10.1126/science.1158799
13. Ebert AD, Yu J, Rose FF et al (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457(7227):277–280. doi:10.1038/nature07677
14. Soldner F, Hockemeyer D, Beard C et al (2009) Parkinson’s disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136(5):964–977. doi:10.1016/j.cell.2009.02.013
15. Osakada F, Jin Z-B, Hirami Y et al (2009) In vitro differentiation of retinal cells from human pluripotent stem cells by small-molecule induction. J Cell Sci 122(Pt 17):3169–3179. doi:10.1242/jcs.050393
16. Choi K-D, Yu J, Smuga-Otto K et al (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27(3):559–567. doi:10.1634/stemcells.2008-0922
17. Ye Z, Zhan H, Mali P et al (2009) Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 114(27):5473–5480. doi:10.1182/blood-2009-04-217406
18. Taura D, Noguchi M, Sone M et al (2009) Adipogenic differentiation of human induced pluripotent stem cells: comparison with that of human embryonic stem cells. FEBS Lett 583(6):1029–1033. doi:10.1016/j.febslet.2009.02.031
19. Tanaka T, Tohyama S, Murata M et al (2009) In vitro pharmacologic testing using human induced pluripotent stem cell-derived cardiomyocytes. Biochem Biophys Res Commun. 385(4):497–502. doi:10.1016/j.bbrc.2009.05.073
20. Yokoo N, Baba S, Kaichi S et al (2009) The effects of cardioactive drugs on cardiomyocytes derived from human induced pluripotent stem cells. Biochem Biophys Res Commun. 387(3):482–488. doi:10.1016/j.bbrc.2009.07.052
21. Zhang J, Wilson GF, Soerens AG et al (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104(4):e30–e41. doi:10.1161/CIRCRESAHA.108.192237
22. Si-Tayeb K, Noto FK, Nagaoka M et al (2010) Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51(1):297–305. doi:10.1002/hep.23354
23. Sullivan GJ, Hay DC, Park I-H et al (2010) Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 51(1):329–335. doi:10.1002/hep.23335
24. Gerbal-Chaloin S, Funakoshi N, Caillaud A, Gondeau C, Champon B, Si-Tayeb K (2014) Human induced pluripotent stem cells in hepatology: beyond the proof of concept. Am J Pathol 184(2):332–347. doi:10.1016/j.ajpath.2013.09.026
25. • Si-Tayeb K, Lemaigre FP, Duncan SA (2010) Organogenesis and development of the liver. Dev Cell 18(2):175–189. doi:10.1016/j.devcel.2010.01.011. This paper reviews the fundamental molecular mechansims that are responsible for liver organogenesis and development which are critical to enhance our understanding and boost the technology of hiPSCs differentiation towards hepatic fate
26. Zaret KS, Grompe M (2008) Generation and regeneration of cells of the liver and pancreas. Science 322(5907):1490–1494. doi:10.1126/science.1161431
27. Lemaigre FP (2009) Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology 137(1):62–79. doi:10.1053/j.gastro.2009.03.035
28. D’Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE (2005) Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23(12):1534–1541. doi:10.1038/nbt1163
29. Song Z, Cai J, Liu Y et al (2009) Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 19(11):1233–1242. doi:10.1038/cr.2009.107
30. DeLaForest A, Nagaoka M, Si-Tayeb K et al (2011) HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells. Development 138(19):4143–4153. doi:10.1242/dev.062547
31. Takayama K, Kawabata K, Nagamoto Y et al (2014) CCAAT/enhancer binding protein-mediated regulation of TGFβ receptor 2 expression determines the hepatoblast fate decision. Development 141:91–100. doi:10.1242/dev.103168
32. Goldman O, Han S, Hamou W et al (2014) Endoderm generates endothelial cells during liver development. Stem Cell Rep 3(4):556–565. doi:10.1016/j.stemcr.2014.08.009
33. Lorenzini S, Gitto S, Grandini E, Andreone P, Bernardi M (2008) Stem cells for end stage liver disease: how far have we got? World J Gastroenterol 14(29):4593–4599. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2738783&tool=pmcentrez&rendertype=abstract. Accessed 18 Aug 2014
34. • Inoue H, Nagata N, Kurokawa H, Yamanaka S (2014) iPS cells: a game changer for future medicine. EMBO J 33(5):409–417. doi:10.1002/embj.201387098. This paper reviews the feasibility of using iPSCs in medicine and addresses the current demands to improve iPSCs technology for disease modeling and cell transplantation
35. Fattahi F, Asgari S, Pournasr B et al (2013) Disease-corrected hepatocyte-like cells from familial hypercholesterolemia-induced pluripotent stem cells. Mol Biotechnol 54(3):863–873. doi:10.1007/s12033-012-9635-3
36. Zhang S, Chen S, Li W et al (2011) Rescue of ATP7B function in hepatocyte-like cells from Wilson’s disease induced pluripotent stem cells using gene therapy or the chaperone drug curcumin. Hum Mol Genet 20(16):3176–3187. doi:10.1093/hmg/ddr223
37. Yusa K, Rashid ST, Strick-Marchand H et al (2011) Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells. Nature 478(7369):391–394. doi:10.1038/nature10424
38. Choi SM, Kim Y, Shim JS et al (2013) Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 57(6):2458–2468. doi:10.1002/hep.26237
39. •• Maetzel D, Sarkar S, Wang H et al (2014) Genetic and chemical correction of cholesterol accumulation and impaired autophagy in hepatic and neural cells derived from Niemann-Pick type C patient-specific iPS Cells. Stem cell Rep 2(6):866–880. doi:10.1016/j.stemcr.2014.03.014. This article describes the feasibility of TALENs-mediated genetic correction of a disease causing mutation in NPC patient-specific hiPSCs as a way to rescue the disease phenotypes and understand the link between the disease specific-LOF mutation and the associated phenotypes
40. Rubin LL (2008) Stem cells and drug discovery: the beginning of a new era? Cell 132(4):549–552. doi:10.1016/j.cell.2008.02.010
41. Yi F, Liu G-H, Izpisua Belmonte JC (2012) Human induced pluripotent stem cells derived hepatocytes: rising promise for disease modeling, drug development and cell therapy. Protein Cell 3(4):246–250. doi:10.1007/s13238-012-2918-4
42. Asgari S, Pournasr B, Salekdeh GH, Ghodsizadeh A, Ott M, Baharvand H (2010) Induced pluripotent stem cells: a new era for hepatology. J Hepatol 53(4):738–751. doi:10.1016/j.jhep.2010.05.009
43. Szkolnicka D, Zhou W, Lucendo-Villarin B, Hay DC (2013) Pluripotent stem cell-derived hepatocytes: potential and challenges in pharmacology. Annu Rev Pharmacol Toxicol 53:147–159. doi:10.1146/annurev-pharmtox-011112-140306
44. Medine CN, Lucendo-Villarin B, Storck C et al (2013) Developing high-fidelity hepatotoxicity models from pluripotent stem cells. Stem Cells Transl Med 2(7):505–509. doi:10.5966/sctm.2012-0138
45. Szkolnicka D, Farnworth SL, Lucendo-Villarin B, Hay DC (2014) Deriving functional hepatocytes from pluripotent stem cells. Curr Protoc Stem Cell Biol 30:1G.5.1–1G.5.12. doi:10.1002/9780470151808.sc01g05s30
46. Yagi H, Tafaleng E, Nagaya M et al (2009) Embryonic and induced pluripotent stem cells as a model for liver disease. Crit Rev Biomed Eng 37(4–5):377–398. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3700621&tool=pmcentrez&rendertype=abstract. Accessed 9 Aug 2014
47. Chun YS, Chaudhari P, Jang Y-Y(2010) Applications of patient-specific induced pluripotent stem cells; focused on disease modeling, drug screening and therapeutic potentials for liver disease. Int J Biol Sci 6(7):796–805. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3005346&tool=pmcentrez&rendertype=abstract
48. Rashid ST, Corbineau S, Hannan N et al (2010) Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest. 120(9):3127–3136. doi:10.1172/JCI43122
49. •• Cayo MA, Cai J, DeLaForest A et al (2012) JD induced pluripotent stem cell-derived hepatocytes faithfully recapitulate the pathophysiology of familial hypercholesterolemia. Hepatology 56(6):2163–2171. doi:10.1002/hep.25871. This article describes the feasibility of using patient-specific hiPSCs to generate FH-hepatocytes which recapitulate key features of the disease and are competent to respond to hepatoselective pharmaceuticals thus providing a platform for the discovery of novel treatments for FH
50. Satoh D, Maeda T, Ito T et al (2013) Establishment and directed differentiation of induced pluripotent stem cells from glycogen storage disease type Ib patient. Genes Cells 18(12):1053–1069. doi:10.1111/gtc.12101
51. Nakamura K, Hirano K, Wu SM (2013) iPS cell modeling of cardiometabolic diseases. J Cardiovasc Transl Res 6(1):46–53. doi:10.1007/s12265-012-9413-4
52. Liras A (2011) Induced human pluripotent stem cells and advanced therapies: future perspectives for the treatment of haemophilia? Thromb Res 128(1):8–13. doi:10.1016/j.thromres.2011.01.010
53. Wu X, Robotham JM, Lee E et al (2012) Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog 8(4):e1002617. doi:10.1371/journal.ppat.1002617
54. Yoshida T, Takayama K, Kondoh M et al (2011) Use of human hepatocyte-like cells derived from induced pluripotent stem cells as a model for hepatocytes in hepatitis C virus infection. Biochem Biophys Res Commun 416(1–2):119–124. doi:10.1016/j.bbrc.2011.11.007
55. Shlomai A, Schwartz RE, Ramanan V et al (2014) Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems. Proc Natl Acad Sci USA 111(33):1–6. doi:10.1073/pnas.1412631111
56. Trapani L, Segatto M, Pallottini V (2012) Regulation and deregulation of cholesterol homeostasis: the liver as a metabolic “power station”. World J Hepatol 4(6):184–190. doi:10.4254/wjh.v4.i6.184
57. Goldstein JL, Brown MS (2009) The LDL receptor. Arterioscler Thromb Vasc Biol 29(4):431–438. doi:10.1161/ATVBAHA.108.179564
58. Faiz F, Hooper AJ, van Bockxmeer FM (2012) Molecular pathology of familial hypercholesterolemia, related dyslipidemias and therapies beyond the statins. Crit Rev Clin Lab Sci 49(1):1–17. doi:10.3109/10408363.2011.646942
59. Go G-W, Mani A (2012) Low-density lipoprotein receptor (LDLR) family orchestrates cholesterol homeostasis. Yale J Biol Med 85(1):19–28. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3313535&tool=pmcentrez&rendertype=abstract. Accessed 22 Aug 2014
60. Rader DJ, Cohen J, Hobbs HH (2003) Monogenic hypercholesterolemia: new insights in pathogenesis and treatment. 111(12):1795–1803. doi:10.1172/JCI18925.Figure
61. Burnett JR, Ravine D, van Bockxmeer FM, Watts GF (2005) Familial hypercholesterolaemia: a look back, a look ahead. Med J Aust 182(11):552–553. http://www.ncbi.nlm.nih.gov/pubmed/15938678. Accessed 19 Aug 2014
62. Goldstein JL, Brown MS (1974) Binding and degradation of low density lipoproteins by cultured human fibroblasts. Comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J Biol Chem 249(16):5153–5162. http://www.ncbi.nlm.nih.gov/pubmed/4368448. Accessed 23 Aug 2014
63. Leigh SEA, Foster AH, Whittall RA, Hubbart CS, Humphries SE (2008) Update and analysis of the University College London low density lipoprotein receptor familial hypercholesterolemia database. Ann Hum Genet 72(Pt 4):485–498. doi:10.1111/j.1469-1809.2008.00436.x
64. Soufi M, Kurt B, Schweer H et al (2009) Genetics and kinetics of familial hypercholesterolemia, with the special focus on FH-(Marburg) p. W556R. Atheroscler Suppl 10(5):5–11. doi:10.1016/S1567-5688(09)71802-1
65. Seidah NG, Prat A (2007) The proprotein convertases are potential targets in the treatment of dyslipidemia. J Mol Med (Berl) 85(7):685–696. doi:10.1007/s00109-007-0172-7
66. Abifadel M, Varret M, Rabès J-P et al (2003) Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat Genet 34(2):154–156. doi:10.1038/ng1161
67. Cohen JC, Boerwinkle E, Mosley TH, Hobbs HH (2006) Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N Engl J Med 354(12):1264–1272. doi:10.1056/NEJMoa054013
68. Marduel M, Carrié A, Sassolas A et al (2010) Molecular spectrum of autosomal dominant hypercholesterolemia in France. Hum Mutat 31(11):E1811–E1824. doi:10.1002/humu.21348
69. Marques-Pinheiro A, Marduel M, Rabès J-P et al (2010) A fourth locus for autosomal dominant hypercholesterolemia maps at 16q22.1. Eur J Hum Genet 18(11):1236–1242. doi:10.1038/ejhg.2010.94
70. Brown M, Goldstein J (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232(4746):34–47. http://www.nobelprize.org/nobel_prizes/medicine/laureates/1985/brown-goldstein-lecture.pdf. Accessed 24 Aug 2014
71. Sniderman AD, De Graaf J, Couture P, Williams K, Kiss RS, Watts GF (2010) Regulation of plasma LDL: the apoB paradigm. Clin Sci (Lond) 118(5):333–339. doi:10.1042/CS20090402
72. Millar JS, Maugeais C, Ikewaki K et al (2005) Complete deficiency of the low-density lipoprotein receptor is associated with increased apolipoprotein B-100 production. Arterioscler Thromb Vasc Biol 25(3):560–565. doi:10.1161/01.ATV.0000155323.18856.a2
73. Rothe M, Modlich U, Schambach A (2013) Biosafety challenges for use of lentiviral vectors in gene therapy. Curr Gene Ther 13(6):453–468. http://www.ncbi.nlm.nih.gov/pubmed/24195603. Accessed 29 Aug 2014
74. Ikonen E (2008) Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 9(2):125–138. doi:10.1038/nrm2336
75. Rosenbaum AI, Maxfield FR (2011) Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J Neurochem 116(5):789–795. doi:10.1111/j.1471-4159.2010.06976.x
76. Schulze H, Sandhoff K (2011) Lysosomal lipid storage diseases. Cold Spring Harb Perspect Biol 3(6):a004804. doi:10.1101/cshperspect.a004804
77. Singh R, Kaushik S, Wang Y et al (2009) Autophagy regulates lipid metabolism. Nature 458(7242):1131–1135. doi:10.1038/nature07976
78. Singh R, Cuervo AM (2012) Lipophagy: connecting autophagy and lipid metabolism. Int J Cell Biol 2012:282041. doi:10.1155/2012/282041
79. Vanier MT (2010) Niemann-Pick disease type C. Orphanet J Rare Dis 5:16. doi:10.1186/1750-1172-5-16
80. Abi-Mosleh L, Infante RE, Radhakrishnan A, Goldstein JL, Brown MS (2009) Cyclodextrin overcomes deficient lysosome-to-endoplasmic reticulum transport of cholesterol in Niemann-Pick type C cells. Proc Natl Acad Sci USA 106(46):19316–19321. doi:10.1073/pnas.0910916106
81. Dianat N, Steichen C, Vallier L, Weber A, Dubart-Kupperschmitt A (2013) Human pluripotent stem cells for modelling human liver diseases and cell therapy. Curr Gene Ther 13(2):120–132. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3882648&tool=pmcentrez&rendertype=abstract
82. Savla JJ, Nelson BC, Perry CN, Adler ED (2014) Induced pluripotent stem cells for the study of cardiovascular disease. J Am Coll Cardiol 64(5):512–519. doi:10.1016/j.jacc.2014.05.038
83. Ding Q, Strong A, Patel KM et al (2014) Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circ Res 115:488–492. doi:10.1161/CIRCRESAHA.115.304351
84. Rashid ST, Alexander GJM (2013) Induced pluripotent stem cells: from Nobel Prizes to clinical applications. J Hepatol 58(3):625–629. doi:10.1016/j.jhep.2012.10.026
85. Lancaster MA, Knoblich JA (2014) Organogenesis in a dish: modeling development and disease using organoid technologies. Science 345(6194):1247125. doi:10.1126/science.1247125
86. Takebe T, Zhang R, Koike H et al (2014) Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. doi:10.1038/nprot.2014.020
87. Schwartz RE, Trehan K, Andrus L et al (2011) Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci USA. doi:10.1073/pnas.1121400109
88. Leung A, Nah SK, Reid W et al (2013) Induced pluripotent stem cell modeling of multisystemic, hereditary transthyretin amyloidosis. Stem cell Rep 1(5):451–463. doi:10.1016/j.stemcr.2013.10.003
89. Isono K, Jono H, Ohya Y et al (2014) Generation of familial amyloidotic polyneuropathy-specific induced pluripotent stem cells. Stem Cell Res. 12(2):574–583. doi:10.1016/j.scr.2014.01.004