Improved retroviral episome transfer of transcription factors enables sustained cell fate modification

Gene Therapy

Volumn 21, Issue 11, 2014, Pages 938-949

  Schott, J W ^a   Hoffmann, D ^a   Maetzig, T ^a   Muller F J ^b   Steinemann, D ^a   Zychlinski, D ^a   Cantz, T ^a   Baum, C ^a   Schambach, A ^a,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Kiel and Lungen Clinic Grosshansdorf   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN VP16; RETROVIRUS VECTOR; TRANSCRIPTION FACTOR SOX2; INTEGRASE; POU5F1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL FATE; DRUG EFFECT; EPIGENETICS; EPISOME; FEMALE; FIBROBLAST; GENE EXPRESSION; GENE TRANSFER; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; LONG TERMINAL REPEAT; ONCOGENE C MYC; PLURIPOTENT STEM CELL; TRANSACTIVATION; TRANSGENE; CELL DIFFERENTIATION; CELL LINE; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; METABOLISM; PLASMID; PROCEDURES; RETROVIRIDAE;

CELL DIFFERENTIATION; CELL LINE; GENETIC VECTORS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTEGRASES; OCTAMER TRANSCRIPTION FACTOR-3; PLASMIDS; RETROVIRIDAE; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 84910142498     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2014.69     Document Type: Article

References (64)

1. Modlich U, Schambach A, Brugman MH, Wicke DC, Knoess S, Li Z et al. Leukemia induction after a single retroviral vector insertion in Evi1 or Prdm16. Leukemia 2008; 22: 1519-1528.
2. Hacein-Bey-Abina S, von Kalle C, Schmidt M, Le Deist F, Wulffraat N, McIntyre E et al. A serious adverse event after successful gene therapy for X-linked severe combined immunode ficiency. N Engl J Med 2003; 348: 255-256.
3. Howe SJ, Mansour MR, Schwarzwaelder K, Bartholomae C, Hubank M, Kempski H et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 2008; 118: 3143-3150.
4. Stein S, Ott MG, Schultze-Strasser S, Jauch A, Burwinkel B, Kinner A et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010; 16: 198-204.
5. Wanisch K, Yanez-Munoz RJ. Integration-deficient lentiviral vectors: a slow coming of age. Mol Ther 2009; 17: 1316-1332.
6. Yu SS, Dan K, Chono H, Chatani E, Mineno J, Kato I. Transient gene expression mediated by integrase-defective retroviral vectors. Biochem Biophys Res Commun 2008; 368: 942-947.
7. Deyle DR, Li Y, Olson EM, Russell DW. Nonintegrating foamy virus vectors. J Virol 2010; 84: 9341-9349.
8. Vargas Jr J, Gusella GL, Najfeld V, Klotman ME, Cara A. Novel integrase-defective lentiviral episomal vectors for gene transfer. Hum Gene Ther 2004; 15: 361-372.
9. Banasik MB, McCray Jr PB. Integrase-defective lentiviral vectors: progress and applications. Gene Therapy 2010; 17: 150-157.
10. Kholodenko BN, Hancock JF, Kolch W. Signalling ballet in space and time. Nat Rev Mol Cell Biol 2010; 11: 414-426.
11. Graf T, Enver T. Forcing cells to change lineages. Nature 2009; 462: 587-594.
12. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987; 51: 987-1000.
13. Xie H, Ye M, Feng R, Graf T. Stepwise reprogramming of B cells into macrophages. Cell 2004; 117: 663-676.
14. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676.
15. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
16. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920.
17. Hockemeyer D, Soldner F, Cook EG, Gao Q, Mitalipova M, Jaenisch R. A drug-inducible system for direct reprogramming of human somatic cells to pluripotency. Cell Stem Cell 2008; 3: 346-353.
18. Feng B, Ng JH, Heng JC, Ng HH. Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell 2009; 4: 301-312.
19. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000; 24: 372-376.
20. Kim J, Efe JA, Zhu S, Talantova M, Yuan X, Wang S et al. Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci USA 2011; 108: 7838-7843.
21. Thier M, Worsdorfer P, Lakes YB, Gorris R, Herms S, Opitz T et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012; 10: 473-479.
22. Szabo E, Rampalli S, Risueno RM, Schnerch A, Mitchell R, Fiebig-Comyn A et al. Direct conversion of human fibroblasts to multilineage blood progenitors. Nature 2010; 468: 521-526.
23. Efe JA, Hilcove S, Kim J, Zhou H, Ouyang K, Wang G et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 2011; 13: 215-222.
24. Schambach A, Bohne J, Baum C, Hermann FG, Egerer L, von Laer D et al. Woodchuck hepatitis virus post-transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Therapy 2006; 13: 641-645.
25. Schneider WM, Wu DT, Amin V, Aiyer S, Roth MJ, MuLV IN. mutants responsive to HDAC inhibitors enhance transcription from unintegrated retroviral DNA. Virology 2012; 426: 188-196.
26. Pelascini LP, Janssen JM, Goncalves MA. Histone deacetylase inhibition activates transgene expression from integration-defective lentiviral vectors in dividing and non-dividing cells. Hum Gene Ther 2013; 24: 78-96.
27. Berger SL, Pina B, Silverman N, Marcus GA, Agapite J, Regier JL et al. Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains. Cell 1992; 70: 251-265.
28. Gilbert DM, Heery DM, Losson R, Chambon P, Lemoine Y. Estradiol-inducible squelching and cell growth arrest by a chimeric VP16-estrogen receptor expressed in Saccharomyces cerevisiae: suppression by an allele of PDR1. Mol Cell Biol 1993; 13: 462-472.
29. Seipel K, Georgiev O, Schaffner W. Different activation domains stimulate transcription from remote ('enhancer') and proximal ('promoter') positions. EMBO J 1992; 11: 4961-4968.
30. Baron U, Gossen M, Bujard H. Tetracycline-controlled transcription in eukaryotes: novel transactivators with graded transactivation potential. Nucleic Acids Res 1997; 25: 2723-2729.
31. Saxe JP, Tomilin A, Scholer HR, Plath K, Huang J. Post-translational regulation of Oct4 transcriptional activity. PLoS One 2009; 4: e4467.
32. Warlich E, Kuehle J, Cantz T, Brugman MH, Maetzig T, Galla M et al. Lentiviral vector design and imaging approaches to visualize the early stages of cellular reprogramming. Mol Ther 2011; 19: 782-789.
33. Hotta A, Ellis J. Retroviral vector silencing during iPS cell induction: an epigenetic beacon that signals distinct pluripotent states. J Cell Biochem 2008; 105: 940-948.
34. Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 2007; 25: 803-816.
35. Müller FJ, Schuldt BM, Williams R, Mason D, Altun G, Papapetrou EP et al. A bioinformatic assay for pluripotency in human cells. Nat Methods 2011; 8: 315-317.
36. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 1992; 89: 5547-5551.
37. Ramos-Mejia V, Montes R, Bueno C, Ayllon V, Real PJ, Rodriguez R et al. Residual expression of the reprogramming factors prevents differentiation of iPSC generated from human fibroblasts and cord blood CD34+ progenitors. PLoS One 2012; 7: e35824.
38. Cronin J, Zhang XY, Reiser J. Altering the tropism of lentiviral vectors through pseudotyping. Curr Gene Ther 2005; 5: 387-398.
39. Funke S, Maisner A, Muhlebach MD, Koehl U, Grez M, Cattaneo R et al. Targeted cell entry of lentiviral vectors. Mol Ther 2008; 16: 1427-1436.
40. Anliker B, Abel T, Kneissl S, Hlavaty J, Caputi A, Brynza J et al. Specific gene transfer to neurons, endothelial cells and hematopoietic progenitors with lentiviral vectors. Nat Methods 2010; 7: 929-935.
41. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009; 324: 797-801.
42. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S et al. A more efficient method to generate integration-free human iPS cells. Nat Methods 2011; 8: 409-412.
43. Zhou W, Freed CR. Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells 2009; 27: 2667-2674.
44. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science 2008; 322: 945-949.
45. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. 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 B2009; 85: 348-362.
46. Seki T, Yuasa S, Oda M, Egashira T, Yae K, Kusumoto D et al. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 2010; 7: 11-14.
47. Tokusumi T, Iida A, Hirata T, Kato A, Nagai Y, Hasegawa M. Recombinant Sendai viruses expressing different levels of a foreign reporter gene. Virus Res 2002; 86: 33-38.
48. Tiemann U, Sgodda M, Warlich E, Ballmaier M, Scholer HR, Schambach A et al. Optimal reprogramming factor stoichiometry increases colony numbers and affects molecular characteristics of murine induced pluripotent stem cells. Cytometry A 2011; 79: 426-435.
49. Zhang Y, Li W, Laurent T, Ding S. Small molecules, big roles-the chemical manipulation of stem cell fate and somatic cell reprogramming. J Cell Sci 2012; 125: 5609-5620.
50. Hirai H, Tani T, Kikyo N. Structure and functions of powerful transactivators: VP16, MyoD and FoxA. Int J Dev Biol 2010; 54: 1589-1596.
51. Wang Y, Chen J, Hu JL, Wei XX, Qin D, Gao J et al. Reprogramming of mouse and human somatic cells by high-performance engineered factors. EMBO Rep 2011; 12: 373-378.
52. Sterneckert J, Hoing S, Scholer HR. Concise review: Oct4 and more: the reprogramming expressway. Stem Cells 2012; 30: 15-21.
53. Murnane JP, Yezzi MJ, Young BR. Recombination events during integration of transfected DNA into normal human cells. Nucleic Acids Res 1990; 18: 2733-2738.
54. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008; 322: 949-953.
55. Jincho Y, Araki R, Hoki Y, Tamura C, Nakamura M, Ando S et al. Generation of genome integration-free induced pluripotent stem cells from fibroblasts of C57BL/6 mice without c-Myc transduction. J Biol Chem 2010; 285: 26384-26389.
56. Gonzalez F, Barragan Monasterio M, Tiscornia G, Montserrat Pulido N, Vassena R, Batlle Morera L et al. Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci USA 2009; 106: 8918-8922.
57. Mali P, Ye Z, Hommond HH, Yu X, Lin J, Chen G et al. Improved efficiency and pace of generating induced pluripotent stem cells from human adult and fetal fibroblasts. Stem Cells 2008; 26: 1998-2005.
58. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V et al. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 2008; 454: 646-650.
59. Rais Y, Zviran A, Geula S, Gafni O, Chomsky E, Viukov S et al. Deterministic direct reprogramming of somatic cells to pluripotency. Nature 2013; 502: 65-70.
60. Schambach A, Bohne J, Chandra S, Will E, Margison GP, Williams DA 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.
61. Schambach A, Mueller D, Galla M, Verstegen MM, Wagemaker G, Loew R et al. Overcoming promoter competition in packaging cells improves production of self-inactivating retroviral vectors. Gene Therapy 2006; 13: 1524-1533.
62. Maetzig T, Galla M, Brugman MH, Loew R, Baum C, Schambach A. Mechanisms controlling titer and expression of bidirectional lentiviral and gammaretroviral vectors. Gene Therapy 2010; 17: 400-411.
63. Heinz N, Schambach A, Galla M, Maetzig T, Baum C, Loew R et al. Retroviral and transposon-based tet-regulated all-in-one vectors with reduced background expression and improved dynamic range. Hum Gene Ther 2011; 22: 166-176.
64. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 2010; 6: 71-79.