Sustained knockdown of a disease-causing gene in patient-specific induced pluripotent stem cells using lentiviral vector-based gene therapy

Stem Cells Translational Medicine

Volumn 2, Issue 9, 2013, Pages 641-654

  Eggenschwiler, Reto ^a   Loya, Komal ^b   Wu, Guangming ^a   Sharma, Amar Deep ^a   Sgodda, Malte ^a   Zychlinski, Daniela ^a   Herr, Christian ^c   Steinemann, Doris ^a   Teckman, Jeffrey ^d   Bals, Robert ^c   Ott, Michael ^a   Schambach, Axel ^a   Scḧler, Hans Robert ^b   Cantz, Tobias ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gene therapy; Hepatocyte differentiation; Lentiviral vector; Liver; Pluripotent stem cells; RNAi

Indexed keywords

COMPLEMENTARY DNA; CYTOCHROME P450 1A1; GENOMIC DNA; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; MICRORNA; MICRORNA 30; RNA POLYMERASE II; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ALPHA 1 ANTITRYPSIN DEFICIENCY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CYTOMEGALOVIRUS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; GENE DOSAGE; GENE SILENCING; GENE THERAPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LIVER INJURY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TRANSGENE;

CYTOMEGALOVIRUS;

EID: 84883394324     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0017     Document Type: Article

References (53)

1. Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: Basic to translational. Biochem J 2012; 443:603-618
2. Papapetrou EP, Lee G, Malani N et al. Genomic safe harbors permit high beta-globin transgene expression in thalassemia induced pluripotent stem cells. Nat Biotechnol 2011; 29:73-78
3. Frimpong K, Spector SA. Cotransduction of nondividing cells using lentiviral vectors. Gene Ther 2000;7:1562-1569
4. Yu X, Zhan X, D'Costa J et al. Lentiviral vectors with two independent internal promoters transfer high-level expression of multiple transgenes to human hematopoietic stem-progenitor cells. Mol Ther 2003;7:827-838
5. Kim D, Kim CH, Moon JI et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009;4:472-476
6. Warren L, Manos PD, Ahfeldt T et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7:618-630
7. Fusaki N, Ban H, Nishiyama A et al. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 2009;85:348-362
8. Chen AA, Thomas DK, Ong LL et al. Humanized mice with ectopic artificial liver tissues. Proc Natl Acad Sci USA 2011;108:11842-11847
9. Khetani SR, Bhatia SN. Microscale culture of human liver cells for drug development. Nat Biotechnol 2008;26:120-126
10. Sveger T. Liver disease in alpha1-antitrypsin deficiency detected by screening of 200,000 infants. N Engl J Med 1976;294:1316-1321
11. Eriksson S, Carlson J, Velez R. Risk of cirrhosis and primary liver cancer in alpha 1-antitrypsin deficiency. N Engl J Med 1986;314: 736-739
12. Hultcrantz R, Mengarelli S. Ultrastructural liver pathology in patients with minimal liver disease and alpha 1-antitrypsin deficiency: A comparison between heterozygous and homozygous patients. Hepatology 1984;4: 937-945
13. Bals R. Alpha-1-antitrypsin deficiency. Best Pract Res Clin Gastroenterol 2010;24: 629-633
14. Eggenschwiler R, Loya K, Sgodda M, et al. Hepatic differentiation of murine disease-specific induced pluripotent stem cells allows disease modelling in vitro. Stem Cells Int 2011; 2011:924782
15. Rashid ST, Corbineau S, Hannan N et al. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 2010;120:3127-3136
16. Schambach A, Bohne J, Chandra S et al. Equal potency of gammaretroviral and lentiviral SIN vectors for expression of O6-methylguanine- DNA methyltransferase in hematopoietic cells. Mol Ther 2006;13:391-400
17. Rudnick DA, Liao Y, An JK et al. Analyses of hepatocellular proliferation in a mouse model of alpha-1-antitrypsin deficiency. Hepatology 2004;39:1048-1055
18. Kim JB, Zaehres H, Wu G et al. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 2008;454:646-650
19. Zhang S, Chen S, Li W 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. Hum Mol Genet 2011;20:3176-3187
20. Wu G, Liu N, Rittelmeyer I et al. Generation of healthy mice from gene-corrected disease- specific induced pluripotent stem cells. PLoS Biol 2011;9:e1001099
21. Li W, Wang X, Fan W et al. Modeling abnormal early development with induced pluripotent stem cells from aneuploid syndromes. Hum Mol Genet 2012;21:32-45
22. Kania G, Blyszczuk P, Jochheim A et al. Generation of glycogen- and albumin-producing hepatocyte-like cells from embryonic stem cells. Biol Chem 2004;385:943-953
23. Sgodda M, Moebus S, Hoepfner J et al. Improved hepatic differentiation strategies for human induced pluripotent stem cells. Curr Mol Med 2013;13:842-855
24. Willenbring H, Sharma AD, Vogel A et al. Loss of p21 permits carcinogenesis from chronically damaged liver and kidney epithelial cells despite unchecked apoptosis. Cancer Cell 2008;14:59-67
25. Ortiz-Pallardo ME, Zhou H, Fischer HP et al. Rapid analysis of alpha1-antitrypsin PiZ genotype by a real-time PCR approach. J MolMed (Berl) 2000;78:212-216
26. Maetzig T, Galla M, Brugman MH et al. Mechanisms controlling titer and expression of bidirectional lentiviral and gammaretroviral vectors. Gene Ther 2010;17:400-411
27. Koczulla AR, Noeske S, Herr C et al. Alpha- 1 antitrypsin is elevated in exhaled breath condensate and serum in exacerbated COPD patients. Respir Med 2012;106:120-126
28. Warlich E, Kuehle J, Cantz T et al. Lentiviral vector design and imaging approaches to visualize the early stages of cellular reprogramming. Mol Ther 2011;19:782-789
29. Pinkert CA, Ornitz DM, Brinster RL et al. An albumin enhancer located 10 kb upstream functions along with its promoter to direct efficient, liver-specific expression in transgenic mice. Genes Dev 1987;1:268-276
30. Sharma AD, Cantz T, Vogel A et al. Murine embryonic stem cell-derived hepatic progenitor cells engraft in recipient livers with limited capacity of liver tissue formation. Cell Transplant 2008;17:313-323
31. Okabe M, Ikawa M, Kominami K et al. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-319
32. Sifers RN, Carlson JA, Clift SM, et al. Tissue specific expression of the human alpha-1-antitrypsin gene in transgenic mice. Nucleic Acids Res 1987;15:1459-1475
33. Carlson JA, Rogers BB, Sifers RN et al. Accumulation of PiZ alpha 1-antitrypsin causes liver damage in transgenic mice. J Clin Invest 1989;83:1183-1190
34. Boden D, Pusch O, Silbermann R et al. Enhanced gene silencing of HIV-1 specific siRNA using microRNA designed hairpins. Nucleic Acids Res 2004;32:1154-1158
35. Suzuki A, Zheng Y, Kondo R et al. Flowcytometric separation and enrichment of hepatic progenitor cells in the developing mouse liver. Hepatology 2000;32:1230-1239
36. Perez P, Adriaansen J, Goldsmith CM et al. Transgenic alpha-1-antitrypsin secreted into the bloodstream from salivary glands is biologically active. Oral Dis 2011;17:476-483
37. Miranda E, Perez J, Ekeowa UI et al. A novel monoclonal antibody to characterize pathogenic polymers in liver disease associated with alpha1-antitrypsin deficiency. Hepatology 2010;52:1078-1088
38. Zou J, Maeder ML, Mali P et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 2009;5:97-110
39. Sebastiano V, Maeder ML, Angstman JF et al. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. STEM CELLS 2011;29:1717-1726
40. Yusa K, Rashid ST, Strick-Marchand H et al. Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 2011;478:391-394
41. Choi SM, Kim Y, Shim JS et al. Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 2013;57:2458-2468
42. Mueller C, Tang Q, Gruntman A et al. Sustained miRNA-mediated knockdown of mutant AAT with simultaneous augmentation of wildtype AAT has minimal effect on global liver miRNA profiles. Mol Ther 2012;20:590-600
43. Inagaki K, Lewis SM, Wu X et al. DNA palindromes with a modest arm length of greater, similar 20 base pairs are a significant target for recombinant adeno-associated virus vector integration in the liver, muscles, and heart in mice. J Virol 2007;81:11290-11303
44. Pastore N, Blomenkamp K, Annunziata F et al. Gene transfer of master autophagy regulator TFEB results in clearance of toxic protein and correction of hepatic disease in alpha-1- anti-trypsin deficiency. EMBO Mol Med 2013; 5:397-412
45. Lombardo A, Cesana D, Genovese P et al. Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat Methods 2011;8:861-869
46. Choi M, Scholl UI, Ji W et al. Genetic diagnosis by whole exome capture and massively parallel DNA sequencing. Proc Natl Acad Sci USA 2009;106:19096-19101
47. He J, Yang Q, Chang LJ. Dynamic DNA methylation and histone modifications contribute to lentiviral transgene silencing in murine embryonic carcinoma cells. J Virol 2005; 79:13497-13508
48. Xu L, Daly T, Gao C et al. CMV-beta-actin promoter directs higher expression from an adeno-associated viral vector in the liver than the cytomegalovirus or elongation factor 1 alpha promoter and results in therapeutic levels of human factor X in mice. Hum Gene Ther 2001;12:563-573
49. Templin C, Zweigerdt R, Schwanke K et al. Transplantation and tracking of human induced pluripotent stem cells in a pig model of myocardial infarction: Assessment of cell survival, engraftment and distribution by hybrid SPECT-CT imaging of sodium iodide symporter transgene expression. Circulation 2012;126: 430-439
50. Berger SM, Pesold B, Reber S et al. Quantitative analysis of conditional gene inactivation using rationally designed, tetracyclinecontrolled miRNAs. Nucleic Acids Res 2010;38: e168
51. Kamata M, Liu S, Liang M et al. Generation of human induced pluripotent stem cells bearing an anti-HIV transgene by a lentiviral vector carrying an internal murine leukemia virus promoter. Hum Gene Ther 2010;21:1555-1567
52. Raya A, Rodriguez-Piza I, Guenechea G et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009;460:53-59
53. Mali P, Yang L, Esvelt KM et al. RNAguided human genome engineering via Cas9. Science 2013;339:823-826.