Integration-deficient lentivectors: An effective strategy to purify and differentiate human embryonic stem cell-derived hepatic progenitors

BMC Biology

Volumn 11, Issue , 2013, Pages

  Yang, Guanghua ^a,b   Si Tayeb, Karim ^a,b   Corbineau, Sébastien ^a,b   Vernet, Rémi ^a   Gayon, Régis ^c   Dianat, Noushin ^a,b   Martinet, Clémence ^a,b   Clay, Denis ^a,b   Goulinet Mainot, Sylvie ^a,b   Tachdjian, Gérard ^e   Burks, Deborah ^d   Vallier, Ludovic ^f   Bouillé, Pascale ^c   Dubart Kupperschmitt, Anne ^a,b   Weber, Anne ^a,b  

^a BICÊTRE HOSPITAL   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Canal Biotech II   (France)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^e HÔPITAL ANTOINE BÉCLÈRE   (France)

^f Stem Cell Biology and Regenerative Medicine   (United Kingdom)

Author keywords

Hepatoblasts; Non integrating lentiviral vectors; Purification; Tissue specific progenitor cells

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRUS;

APOLIPOPROTEIN A2; BIOLOGICAL MARKER; CYP3A4 PROTEIN, HUMAN; CYTOCHROME P450 3A; GREEN FLUORESCENT PROTEIN; VIRUS DNA;

ANTIBODY SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CYTOLOGY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; LENTIVIRINAE; LIVER; LIVER CELL; METABOLISM; METHODOLOGY; PHYSIOLOGY; PROMOTER REGION; REPORTER GENE; VIRUS DNA CELL DNA INTERACTION;

APOLIPOPROTEIN A-II; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CYTOCHROME P-450 CYP3A; DNA, VIRAL; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; HUMANS; LENTIVIRUS; LIVER; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; TRANSDUCTION, GENETIC; VIRUS INTEGRATION;

EID: 84880336102     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-86     Document Type: Article

References (33)

1. Dhawan A, Puppi J, Hughes RD, Mitry RR. Human hepatocyte transplantation: current experience and future challenges. Nat Rev Gastroenterol Hepatol 2010, 7:288-298. 10.1038/nrgastro.2010.44, 20368738.
2. Duan Y, Ma X, Zou W, Wang C, Bahbahan IS, Ahuja TP, Tolstikov V, Zern MA. Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells 2010, 28:674-686. 10.1002/stem.315, 20135682.
3. Hay DC, Zhao D, Fletcher J, Hewitt ZA, McLean D, Urruticoechea-Uriguen A, Black JR, Elcombe C, Ross JA, Wolf R, Cui W. Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells 2008, 26:894-902. 10.1634/stemcells.2007-0718, 18238852.
4. Si-Tayeb K, Noto FK, Nagaoka M, Li J, Battle MA, Duris C, North PE, Dalton S, Duncan SA. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010, 51:297-305. 10.1002/hep.23354, 2946078, 19998274.
5. Sullivan GJ, Hay DC, Park IH, Fletcher J, Hannoun Z, Payne CM, Dalgetty D, Black JR, Ross JA, Samuel K, et al. Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 2010, 51:329-335. 10.1002/hep.23335, 2799548, 19877180.
6. Takayama K, Inamura M, Kawabata K, Katayama K, Higuchi M, Tashiro K, Nonaka A, Sakurai F, Hayakawa T, Furue MK, Mizuguchi H. Efficient generation of functional hepatocytes from human embryonic stem cells and induced pluripotent stem cells by HNF4alpha transduction. Mol Ther 2012, 20:127-137. 10.1038/mt.2011.234, 3255576, 22068426.
7. Touboul T, Hannan NR, Corbineau S, Martinez A, Martinet C, Branchereau S, Mainot S, Strick-Marchand H, Pedersen R, Di Santo J, et al. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 2010, 51:1754-1765. 10.1002/hep.23506, 20301097.
8. Schmelzer E, Zhang L, Bruce A, Wauthier E, Ludlow J, Yao HL, Moss N, Melhem A, McClelland R, Turner W, et al. Human hepatic stem cells from fetal and postnatal donors. J Exp Med 2007, 204:1973-1987. 10.1084/jem.20061603, 2118675, 17664288.
9. Lu TY, Lu RM, Liao MY, Yu J, Chung CH, Kao CF, Wu HC. Epithelial cell adhesion molecule regulation is associated with the maintenance of the undifferentiated phenotype of human embryonic stem cells. J Biol Chem 2010, 285:8719-8732. 10.1074/jbc.M109.077081, 2838295, 20064925.
10. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, Jia H, Ye Q, Qin LX, Wauthier E, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 2009, 136:1012-1024. 10.1053/j.gastro.2008.12.004, 2828822, 19150350.
11. Wanisch K, Yanez-Munoz RJ. Integration-deficient lentiviral vectors: a slow coming of age. Mol Ther 2009, 17:1316-1332. 10.1038/mt.2009.122, 2835240, 19491821.
12. Dagher I, Nguyen TH, Groyer-Picard MT, Lainas P, Mainot S, Guettier C, Pariente D, Franco D, Weber A. Efficient hepatocyte engraftment and long-term transgene expression after reversible portal embolization in nonhuman primates. Hepatology 2009, 49:950-959. 10.1002/hep.22739, 19152424.
13. Parouchev A, Nguyen TH, Dagher I, Mainot S, Groyer-Picard MT, Branger J, Gonin P, Di Santo J, Franco D, Gras G, Weber A. Efficient ex vivo gene transfer into non-human primate hepatocytes using HIV-1 derived lentiviral vectors. J Hepatol 2006, 45:99-107. 10.1016/j.jhep.2006.03.014, 16723167.
14. Banasik MB, McCray PB. Integrase-defective lentiviral vectors: progress and applications. Gene Ther 2010, 17:150-157. 10.1038/gt.2009.135, 19847206.
15. Yanez-Munoz RJ, Balaggan KS, MacNeil A, Howe SJ, Schmidt M, Smith AJ, Buch P, MacLaren RE, Anderson PN, Barker SE, et al. Effective gene therapy with nonintegrating lentiviral vectors. Nat Med 2006, 12:348-353. 10.1038/nm1365, 16491086.
16. Hazuda DJ, Felock P, Witmer M, Wolfe A, Stillmock K, Grobler JA, Espeseth A, Gabryelski L, Schleif W, Blau C, Miller MD. Inhibitors of strand transfer that prevent integration and inhibit HIV-1 replication in cells. Science 2000, 287:646-650. 10.1126/science.287.5453.646, 10649997.
17. Drocourt L, Ourlin JC, Pascussi JM, Maurel P, Vilarem MJ. Expression of CYP3A4, CYP2B6, and CYP2C9 is regulated by the vitamin D receptor pathway in primary human hepatocytes. J Biol Chem 2002, 277:25125-25132. 10.1074/jbc.M201323200, 11991950.
18. Blin G, Nury D, Stefanovic S, Neri T, Guillevic O, Brinon B, Bellamy V, Rucker-Martin C, Barbry P, Bel A, et al. A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates. J Clin Invest 2010, 120:1125-1139. 10.1172/JCI40120, 2846046, 20335662.
19. Hedlund E, Pruszak J, Ferree A, Vinuela A, Hong S, Isacson O, Kim KS. Selection of embryonic stem cell-derived enhanced green fluorescent protein-positive dopamine neurons using the tyrosine hydroxylase promoter is confounded by reporter gene expression in immature cell populations. Stem Cells 2007, 25:1126-1135. 10.1634/stemcells.2006-0540, 2614084, 17234989.
20. Sena-Esteves M, Tebbets JC, Steffens S, Crombleholme T, Flake AW. Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 2004, 122:131-139. 10.1016/j.jviromet.2004.08.017, 15542136.
21. Bally-Cuif L, Goutel C, Wassef M, Wurst W, Rosa F. Coregulation of anterior and posterior mesendodermal development by a hairy-related transcriptional repressor. Genes Dev 2000, 14:1664-1677. 316738, 10887160.
22. Tada S, Era T, Furusawa C, Sakurai H, Nishikawa S, Kinoshita M, Nakao K, Chiba T. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 2005, 132:4363-4374. 10.1242/dev.02005, 16141227.
23. Lemaigre F, Zaret KS. Liver development update: new embryo models, cell lineage control, and morphogenesis. Curr Opin Genet Dev 2004, 14:582-590. 10.1016/j.gde.2004.08.004, 15380251.
24. Lemaigre FP. Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology 2009, 137:62-79. 10.1053/j.gastro.2009.03.035, 19328801.
25. Mahieu-Caputo D, Allain JE, Branger J, Coulomb A, Delgado JP, Andreoletti M, Mainot S, Frydman R, Leboulch P, Di Santo JP, et al. Repopulation of athymic mouse liver by cryopreserved early human fetal hepatoblasts. Hum Gene Ther 2004, 15:1219-1228. 10.1089/hum.2004.15.1219, 15684698.
26. Turner R, Lozoya O, Wang Y, Cardinale V, Gaudio E, Alpini G, Mendel G, Wauthier E, Barbier C, Alvaro D, Reid LM. Human hepatic stem cell and maturational liver lineage biology. Hepatology 2011, 53:1035-1045. 10.1002/hep.24157, 3066046, 21374667.
27. Hannan NR, Segeritz CP, Touboul T, Vallier L. Production of hepatocyte-like cells from human pluripotent stem cells. Nat Protoc 2013, 8:430-437. 10.1038/nprot.2012.153, 3673228, 23424751.
28. Engelman A, Mizuuchi K, Craigie R. HIV-1 DNA integration: mechanism of viral DNA cleavage and DNA strand transfer. Cell 1991, 67:1211-1221. 10.1016/0092-8674(91)90297-C, 1760846.
29. Matrai J, Cantore A, Bartholomae CC, Annoni A, Wang W, Acosta-Sanchez A, Samara-Kuko E, De Waele L, Ma L, Genovese P, et al. Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice with low genotoxic risk. Hepatology 2011, 53:1696-1707. 10.1002/hep.24230, 3112259, 21520180.
30. Eron JJ, Rockstroh JK, Reynes J, Andrade-Villanueva J, Ramalho-Madruga JV, Bekker LG, Young B, Katlama C, Gatell-Artigas JM, Arribas JR, et al. Raltegravir once daily or twice daily in previously untreated patients with HIV-1: a randomised, active-controlled, phase 3 non-inferiority trial. Lancet Infect Dis 2011, 11:907-915. 10.1016/S1473-3099(11)70196-7, 21933752.
31. Villa-Diaz LG, Ross AM, Lahann J, Krebsbach PH. Concise review: The evolution of human pluripotent stem cell culture: from feeder cells to synthetic coatings. Stem Cells 2013, 31:1-7. 10.1002/stem.1260, 23081828.
32. Allain JE, Dagher I, Mahieu-Caputo D, Loux N, Andreoletti M, Westerman K, Briand P, Franco D, Leboulch P, Weber A. Immortalization of a primate bipotent epithelial liver stem cell. Proc Natl Acad Sci USA 2002, 99:3639-3644. 10.1073/pnas.062038599, 122576, 11904425.
33. Mcmanus JF. The effect of various solvents and other conditions on periodate oxidation of carbohydrates in the PAS reaction. Ann Histochim. 1962, 7:57-9.