Detailed comparison of retroviral vectors and promoter configurations for stable and high transgene expression in human induced pluripotent stem cells

Gene Therapy

Volumn 24, Issue 5, 2017, Pages 298-307

  Hoffmann, D ^a   Schott, J W ^a   Geis, F K ^a   Lange, L ^a   Muller F J ^b   Lenz, D ^a   Zychlinski, D ^a   Steinemann, D ^a   Morgan, M ^a   Moritz, T ^a   Schambach, A ^a,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1ALPHA; LENTIVIRUS VECTOR; RETROVIRUS VECTOR; VIRUS GLYCOPROTEIN; ELONGATION FACTOR 1;

ALPHARETROVIRUS; ARTICLE; CELL DIFFERENTIATION; CHROMATIN; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG POTENCY; ENDOTHELIUM CELL; FIBROBLAST; GAMMARETROVIRUS; GENE CASSETTE; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE SILENCING; GENE TRANSFER; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROMOTER REGION; RETROVIRIDAE; SPLEEN FOCUS FORMING VIRUS; TRANSGENE; VESICULOVIRUS; VIRAL GENE DELIVERY SYSTEM; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS TITRATION; CELL CULTURE; CYTOLOGY; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; METABOLISM; PROCEDURES; STANDARDS;

CELLS, CULTURED; ENDOTHELIAL CELLS; GENE SILENCING; GENETIC VECTORS; HELA CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; PEPTIDE ELONGATION FACTOR 1; PROMOTER REGIONS, GENETIC; RETROVIRIDAE; TRANSFECTION; TRANSGENES;

EID: 85019906447     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2017.20     Document Type: Article

References (53)

1. Schambach A, Cantz T, Baum C, Cathomen T. Generation and genetic modification of induced pluripotent stem cells. Expert Opin Biol Ther 2010; 10: 1089-1103.
2. Cherry AB, Daley GQ. Reprogrammed cells for disease modeling and regenerative medicine. Annu Rev Med 2013; 64: 277-290.
3. Ellis J. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum Gene Ther 2005; 16: 1241-1246.
4. Mok HP, Javed S, Lever A. Stable gene expression occurs from a minority of integrated HIV-1-based vectors: transcriptional silencing is present in the majority. Gene Ther 2007; 14: 741-751.
5. Minoguchi S, Iba H. Instability of retroviral DNA methylation in embryonic stem cells. Stem Cells 2008; 26: 1166-1173.
6. Herbst F, Ball CR, Tuorto F, Nowrouzi A, Wang W, Zavidij O et al. Extensive methylation of promoter sequences silences lentiviral transgene expression during stem cell differentiation in vivo. Mol Ther 2012; 20: 1014-1021.
7. Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 2007; 131: 46-57.
8. Schlesinger S, Lee AH, Wang GZ, Green L, Goff SP. Proviral silencing in embryonic cells is regulated by Yin Yang 1. Cell Rep 2013; 4: 50-58.
9. Wolf D, Goff SP. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009; 458: 1201-1204.
10. Grez M, Akgun E, Hilberg F, Ostertag W. Embryonic stem cell virus, a recombinant murine retrovirus with expression in embryonic stem cells. Proc Natl Acad Sci USA 1990; 87: 9202-9206.
11. Ramezani A, Hawley TS, Hawley RG. Lentiviral vectors for enhanced gene expression in human hematopoietic cells. Mol Ther 2000; 2: 458-469.
12. Ramezani A, Hawley TS, Hawley RG. Stable gammaretroviral vector expression during embryonic stem cell-derived in vitro hematopoietic development. Mol Ther 2006; 14: 245-254.
13. Antoniou MN, Skipper KA, Anakok O. Optimizing retroviral gene expression for effective therapies. Hum Gene Ther 2013; 24: 363-374.
14. Emery DW. The use of chromatin insulators to improve the expression and safety of integrating gene transfer vectors. Hum Gene Ther 2011; 22: 761-774.
15. Antoniou M, Harland L, Mustoe T, Williams S, Holdstock J, Yague E et al. Transgenes encompassing dual-promoter CpG islands from the human TBP and HNRPA2B1 loci are resistant to heterochromatin-mediated silencing. Genomics 2003; 82: 269-279.
16. Urbinati F, Arumugam P, Higashimoto T, Perumbeti A, Mitts K, Xia P et al. Mechanism of reduction in titers from lentivirus vectors carrying large inserts in the 3'LTR. Mol Ther 2009; 17: 1527-1536.
17. Puthenveetil G, Scholes J, Carbonell D, Qureshi N, Xia P, Zeng L et al. Successful correction of the human beta-thalassemia major phenotype using a lentiviral vector. Blood 2004; 104: 3445-3453.
18. Sharma N, Hollensen AK, Bak RO, Staunstrup NH, Schroder LD, Mikkelsen JG. The impact of cHS4 insulators on DNA transposon vector mobilization and silencing in retinal pigment epithelium cells. PloS One 2012; 7: e48421.
19. Zhang F, Thornhill SI, Howe SJ, Ulaganathan M, Schambach A, Sinclair J et al. Lentiviral vectors containing an enhancer-less ubiquitously acting chromatin opening element (UCOE) provide highly reproducible and stable transgene expression in hematopoietic cells. Blood 2007; 110: 1448-1457.
20. Zhang F, Frost AR, Blundell MP, Bales O, Antoniou MN, Thrasher AJ. A ubiquitous chromatin opening element (UCOE) confers resistance to DNA methylationmediated silencing of lentiviral vectors. Mol Ther 2010; 18: 1640-1649.
21. Pfaff N, Lachmann N, Ackermann M, Kohlscheen S, Brendel C, Maetzig T et al. A ubiquitous chromatin opening element prevents transgene silencing in pluripotent stem cells and their differentiated progeny. Stem Cells 2013; 31: 488-499.
22. Ackermann M, Lachmann N, Hartung S, Eggenschwiler R, Pfaff N, Happle C et al. Promoter and lineage independent anti-silencing activity of the A2 ubiquitous chromatin opening element for optimized human pluripotent stem cell-based gene therapy. Biomaterials 2014; 35: 1531-1542.
23. Muller-Kuller U, Ackermann M, Kolodziej S, Brendel C, Fritsch J, Lachmann N et al. A minimal ubiquitous chromatin opening element (UCOE) effectively prevents silencing of juxtaposed heterologous promoters by epigenetic remodeling in multipotent and pluripotent stem cells. Nucleic Acids Res 2015; 43: 1577-1592.
24. 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.
25. Voelkel C, Galla M, Maetzig T, Warlich E, Kuehle J, Zychlinski D et al. Protein transduction from retroviral Gag precursors. Proc Natl Acad USA 2010; 107: 7805-7810.
26. Kaufmann KB, Brendel C, Suerth JD, Mueller-Kuller U, Chen-Wichmann L, Schwable J et al. Alpharetroviral vector-mediated gene therapy for X-CGD: functional correction and lack of aberrant splicing. Mol Ther 2013; 21: 648-661.
27. Suerth JD, Morgan MA, Kloess S, Heckl D, Neudorfl C, Falk CS et al. Efficient generation of gene-modified human natural killer cells via alpharetroviral vectors. J Mol Med 2016; 94: 83-93.
28. Labenski V, Suerth JD, Barczak E, Heckl D, Levy C, Bernadin O et al. Alpharetroviral self-inactivating vectors produced by a superinfection-resistant stable packaging cell line allow genetic modification of primary human T lymphocytes. Biomaterials 2016; 97: 97-109.
29. Suerth JD, Maetzig T, Brugman MH, Heinz N, Appelt JU, Kaufmann KB et al. Alpharetroviral self-inactivating vectors: long-term transgene expression in murine hematopoietic cells and low genotoxicity. Mol Ther 2012; 20: 1022-1032.
30. Hacein-Bey-Abina S, Pai SY, Gaspar HB, Armant M, Berry CC, Blanche S et al. A modified gamma-retrovirus vector for X-linked severe combined immunodeficiency. N Engl J Med 2014; 371: 1407-1417.
31. Aiuti A, Biasco L, Scaramuzza S, Ferrua F, Cicalese MP, Baricordi C et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013; 341: 1233151.
32. Naldini L. Gene therapy returns to centre stage. Nature 2015; 526: 351-360.
33. Raya A, Rodriguez-Piza I, Guenechea G, Vassena R, Navarro S, Barrero MJ et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009; 460: 53-59.
34. Lachmann N, Happle C, Ackermann M, Luttge D, Wetzke M, Merkert S et al. Gene correction of human induced pluripotent stem cells repairs the cellular phenotype in pulmonary alveolar proteinosis. Am J Respir Crit Care Med 2014; 189: 167-182.
35. Papapetrou EP, Lee G, Malani N, Setty M, Riviere I, Tirunagari LM et al. Genomic safe harbors permit high beta-globin transgene expression in thalassemia induced pluripotent stem cells. Nat Biotechnol 2010; 29: 73-78.
36. Morishima T, Watanabe K, Niwa A, Hirai H, Saida S, Tanaka T et al. Genetic correction of HAX1 in induced pluripotent stem cells from a patient with severe congenital neutropenia improves defective granulopoiesis. Haematologica 2014; 99: 19-27.
37. Finkelshtein D, Werman A, Novick D, Barak S, Rubinstein M. LDL receptor and its family members serve as the cellular receptors for vesicular stomatitis virus. Proc Natl Acad Sci USA 2013; 110: 7306-7311.
38. Amirache F, Levy C, Costa C, Mangeot PE, Torbett BE, Wang CX et al. Mystery solved: VSV-G-LVs do not allow efficient gene transfer into unstimulated T cells, B cells, and HSCs because they lack the LDL receptor. Blood 2014; 123: 1422-1424.
39. Rasko JE, Battini JL, Gottschalk RJ, Mazo I, Miller AD. The RD114/simian type D retrovirus receptor is a neutral amino acid transporter. Proc Natl Acad Sci USA 1999; 96: 2129-2134.
40. Norrman K, Fischer Y, Bonnamy B, Wolfhagen Sand F, Ravassard P, Semb H. Quantitative comparison of constitutive promoters in human ES cells. PloS One 2010; 5: e12413.
41. Rival-Gervier S, Lo MY, Khattak S, Pasceri P, Lorincz MC, Ellis J. Kinetics and epigenetics of retroviral silencing in mouse embryonic stem cells defined by deletion of the D4Z4 element. Mol Ther 2013; 21: 1536-1550.
42. Papapetrou EP, Schambach A. Gene insertion into genomic safe harbors for human gene therapy. Mol Ther 2016; 24: 678-684.
43. Ordovas L, Boon R, Pistoni M, Chen Y, Wolfs E, Guo W et al. Efficient recombinasemediated cassette exchange in hPSCs to study the hepatocyte lineage reveals AAVS1 locus-mediated transgene inhibition. Stem Cell Rep 2015; 5: 918-931.
44. Kuehle J, Turan S, Cantz T, Hoffmann D, Suerth JD, Maetzig T et al. Modified lentiviral LTRs allow Flp recombinase-mediated cassette exchange and in vivo tracing of "Factor-free" induced pluripotent stem cells. Mol Ther 2014; 22: 919-928.
45. Suerth JD, Maetzig T, Galla M, Baum C, Schambach A. Self-inactivating alpharetroviral vectors with a split-packaging design. J Virol 2010; 84: 6626-6635.
46. 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.
47. 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 Ther 2006; 13: 1524-1533.
48. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998; 72: 8463-8471.
49. Schott JW, Hoffmann D, Maetzig T, Muller FJ, Steinemann D, Zychlinski D et al. Improved retroviral episome transfer of transcription factors enables sustained cell fate modification. Gene Ther 2014; 21: 938-949.
50. Yee JK, Friedmann T, Burns JC. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 1994; 43: 99-112.
51. Cone RD, Mulligan RC. High-efficiency gene transfer into mammalian cells: generation of helper-free recombinant retrovirus with broad mammalian host range. Proc Natl Acad Sci USA 1984; 81: 6349-6353.
52. Sandrin V, Boson B, Salmon P, Gay W, Negre D, Le Grand R et al. Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood 2002; 100: 823-832.
53. Orlova VV, Drabsch Y, Freund C, Petrus-Reurer S, van den Hil FE, Muenthaisong S et al. Functionality of endothelial cells and pericytes from human pluripotent stem cells demonstrated in cultured vascular plexus and zebrafish xenografts. Arterioscler Thromb Vasc Biol 2014; 34: 177-186.