Generation of induced pluripotent stem cells from human foetal fibroblasts using the Sleeping Beauty transposon gene delivery system

Differentiation

Volumn 86, Issue 1-2, 2013, Pages 30-37

  Davis, Richard P ^a,b   Nemes, Csilla ^d   Varga, Eszter ^c,d   Freund, Christian ^a   Kosmidis, Georgios ^a   Gkatzis, Konstantinos ^a   de Jong, Danielle ^a   Szuhai, Károly ^a   Dinnyés, András ^c,d   Mummery, Christine L ^a,b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Netherlands Proteomics Institute   (Netherlands)

^c SZENT ISTVÁN UNIVERSITY   (Hungary)

^d BIOTALENTUM LTD   (Hungary)

Author keywords

Differentiation; Human Induced pluripotent stem cell; Nuclear reprogramming; Sleeping Beauty transposon; Transfection methods

Indexed keywords

TRANSPOSASE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FETUS; FIBROBLAST; GENE DELIVERY SYSTEM; GERM LAYER; HUMAN; HUMAN CELL; HUMAN GENOME; IN VITRO STUDY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SLEEPING BEAUTY TRANSPOSON; TRANSPOSON;

DIFFERENTIATION; HUMAN INDUCED PLURIPOTENT STEM CELL; NUCLEAR REPROGRAMMING; SLEEPING BEAUTY TRANSPOSON; TRANSFECTION METHODS;

CELL DIFFERENTIATION; CELLS, CULTURED; DNA TRANSPOSABLE ELEMENTS; EMBRYONIC STEM CELLS; FIBROBLASTS; GENE TRANSFER TECHNIQUES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NUCLEAR REPROGRAMMING;

EID: 84882660765     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2013.06.002     Document Type: Article

References (45)

1. Bellin M., Marchetto M.C., Gage F.H., Mummery C.L. Induced pluripotent stem cells: the new patient?. Nat. Rev. Mol. Cell Biol. 2012, 13:713-726.
2. Cadinanos J., Bradley A. Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res. 2007, 35:e87.
3. Costa M., Sourris K., Hatzistavrou T., Elefanty A.G., Stanley E.G. Expansion of human embryonic stem cells in vitro. Curr. Protocols Stem Cell Biol. 2007, 1. 1C.1.1-1C.1.7.
4. Davis R.P., Casini S., van den Berg C.W., Hoekstra M., Remme C.A., Dambrot C., Salvatori D., Ward-van Oostwaard D., Wilde A.A., Bezzina C.R., Verkerk A.O., Freund C., Mummery C.L. Cardiomyocytes derived from pluripotent stem cells recapitulate electrophysiological characteristics of an overlap syndrome of cardiac sodium channel disease. Circulation 2012, 125:3079-3091.
5. Davis R.P., Grandela C., Sourris K., Hatzistavrou T., Dottori M., Elefanty A.G., Stanley E.G., Costa M. Generation of human embryonic stem cell reporter knock-in lines by homologous recombination. Curr. Protocols Stem Cell Biol. 2009, 11. 5B.1.1-5B.1.34.
6. Davis R.P., van den Berg C.W., Casini S., Braam S.R., Mummery C.L. Pluripotent stem cell models of cardiac disease and their implication for drug discovery and development. Trends Mol. Med. 2011, 17:475-484.
7. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., Wichterle H., Henderson C.E., Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
8. Foster K.W., Liu Z., Nail C.D., Li X., Fitzgerald T.J., Bailey S.K., Frost A.R., Louro I.D., Townes T.M., Paterson A.J., Kudlow J.E., Lobo-Ruppert S.M., Ruppert J.M. Induction of KLF4 in basal keratinocytes blocks the proliferation-differentiation switch and initiates squamous epithelial dysplasia. Oncogene 2005, 24:1491-1500.
9. Freund C., Ward-van Oostwaard D., Monshouwer-Kloots J., van den Brink S., van Rooijen M., Xu X., Zweigerdt R., Mummery C., Passier R. Insulin redirects differentiation from cardiogenic mesoderm and endoderm to neuroectoderm in differentiating human embryonic stem cells. Stem Cells 2008, 26:724-733.
10. 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. B Phys. Biol. Sci. 2009, 85:348-362.
11. Gonzalez F., Boue S., Izpisua Belmonte J.C. Methods for making induced pluripotent stem cells: reprogramming a la carte. Nat. Rev. Genet. 2011, 12:231-242.
12. Grabundzija I., Wang J., Sebe A., Erdei Z., Kajdi R., Devaraj A., Steinemann D., Szuhai K., Stein U., Cantz T., Schambach A., Baum C., Izsvak Z., Sarkadi B., Ivics Z. Sleeping Beauty transposon-based system for cellular reprogramming and targeted gene insertion in induced pluripotent stem cells. Nucleic Acids Res. 2013, 41:1829-1847.
13. Hackett P.B., Largaespada D.A., Cooper L.J. A transposon and transposase system for human application. Mol. Ther. 2010, 18:674-683.
14. Hawley R.G. Does retroviral insertional mutagenesis play a role in the generation of induced pluripotent stem cells?. Mol. Ther. 2008, 16:1354-1355.
15. Hochedlinger K., Yamada Y., Beard C., Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 2005, 121:465-477.
16. 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.
17. Ivics Z., Hackett P.B., Plasterk R.H., Izsvak Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 1997, 91:501-510.
18. Ivics Z., Izsvak Z. Nonviral gene delivery with the Sleeping Beauty transposon system. Hum. Gene Ther. 2011, 22:1043-1051.
19. Izsvak Z., Frohlich J., Grabundzija I., Shirley J.R., Powell H.M., Chapman K.M., Ivics Z., Hamra F.K. Generating knockout rats by transposon mutagenesis in spermatogonial stem cells. Nat. Methods 2010, 7:443-445.
20. Jia F., Wilson K.D., Sun N., Gupta D.M., Huang M., Li Z., Panetta N.J., Chen Z.Y., Robbins R.C., Kay M.A., Longaker M.T., Wu J.C. A nonviral minicircle vector for deriving human iPS cells. Nat. Methods 2010, 7:197-199.
21. Kaji K., Norrby K., Paca A., Mileikovsky M., Mohseni P., Woltjen K. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 2009, 458:771-775.
22. Lowry W.E., Richter L., Yachechko R., Pyle A.D., Tchieu J., Sridharan R., Clark A.T., Plath K. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc. Natl. Acad. Sci. USA 2008, 105:2883-2888.
23. Luo G., Ivics Z., Izsvak Z., Bradley A. Chromosomal transposition of a Tc1/mariner-like element in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 1998, 95:10769-10773.
24. Mandal P.K., Rossi D.J. Reprogramming human fibroblasts to pluripotency using modified mRNA. Nat. Protocols 2013, 8:568-582.
25. Mates L., Chuah M.K., Belay E., Jerchow B., Manoj N., Acosta-Sanchez A., Grzela D.P., Schmitt A., Becker K., Matrai J., Ma L., Samara-Kuko E., Gysemans C., Pryputniewicz D., Miskey C., Fletcher B., VandenDriessche T., Ivics Z., Izsvak Z. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 2009, 41:753-761.
26. Muenthaisong S., Ujhelly O., Polgar Z., Varga E., Ivics Z., Pirity M.K., Dinnyes A. Generation of mouse induced pluripotent stem cells from different genetic backgrounds using Sleeping Beauty transposon mediated gene transfer. Exp. Cell Res. 2012, 318:2482-2489.
27. Nakagawa M., Koyanagi M., Tanabe K., Takahashi K., Ichisaka T., Aoi T., Okita K., Mochiduki Y., Takizawa N., Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol. 2008, 26:101-106.
28. Ng E.S., Davis R.P., Stanley E.G., Elefanty A.G. A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat. Protocols 2008, 3:768-776.
29. Schroder A.R., Shinn P., Chen H., Berry C., Ecker J.R., Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002, 110:521-529.
30. Soldner F., Hockemeyer D., Beard C., Gao Q., Bell G.W., Cook E.G., Hargus G., Blak A., Cooper O., Mitalipova M., Isacson O., Jaenisch R. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009, 136:964-977.
31. Sommer C.A., Sommer A.G., Longmire T.A., Christodoulou C., Thomas D.D., Gostissa M., Alt F.W., Murphy G.J., Kotton D.N., Mostoslavsky G. Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells 2010, 28:64-74.
32. Staerk J., Dawlaty M.M., Gao Q., Maetzel D., Hanna J., Sommer C.A., Mostoslavsky G., Jaenisch R. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010, 7:20-24.
33. Szuhai K., Tanke H.J. COBRA: combined binary ratio labeling of nucleic-acid probes for multi-color fluorescence in situ hybridization karyotyping. Nat. Protocols 2006, 1:264-275.
34. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
35. Uren A.G., Mikkers H., Kool J., Van Der Weyden L., Lund A.H., Wilson C.H., Rance R., Jonkers J., Van Lohuizen M., Berns A., Adams D.J. A high-throughput splinkerette-PCR method for the isolation and sequencing of retroviral insertion sites. Nat. Protocols 2009, 4:789-798.
36. VandenDriessche T., Ivics Z., Izsvak Z., Chuah M.K. Emerging potential of transposons for gene therapy and generation of induced pluripotent stem cells. Blood 2009, 114:1461-1468.
37. Walisko O., Schorn A., Rolfs F., Devaraj A., Miskey C., Izsvak Z., Ivics Z. Transcriptional activities of the Sleeping Beauty transposon and shielding its genetic cargo with insulators. Mol. Ther. 2008, 16:359-369.
38. Warren L., Manos P.D., Ahfeldt T., Loh Y.H., Li H., Lau F., Ebina W., Mandal P.K., Smith Z.D., Meissner A., Daley G.Q., Brack A.S., Collins J.J., Cowan C., Schlaeger T.M., Rossi D.J. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010, 7:618-630.
39. Wilson M.H., Coates C.J., George A.L. piggyBac Transposon-mediated gene transfer in human cells. Mol. Ther. 2007, 15:139-145.
40. Winkler T., Cantilena A., Metais J.Y., Xu X., Nguyen A.D., Borate B., Antosiewicz-Bourget J.E., Wolfsberg T.G., Thomson J.A., Dunbar C.E. No evidence for clonal selection due to lentiviral integration sites in human induced pluripotent stem cells. Stem Cells 2010, 28:687-694.
41. Woltjen K., Michael I.P., Mohseni P., Desai R., Mileikovsky M., Hamalainen R., Cowling R., Wang W., Liu P., Gertsenstein M., Kaji K., Sung H.K., Nagy A. piggyBac Transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 2009, 458:766-770.
42. Wu S.M., Hochedlinger K. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat. Cell Biol. 2011, 13:497-505.
43. Wu X., Li Y., Crise B., Burgess S.M. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003, 300:1749-1751.
44. Yu J., Hu K., Smuga-Otto K., Tian S., Stewart R., Slukvin, Thomson J.A. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009, 324:797-801.
45. Yusa K., Rad R., Takeda J., Bradley A. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat. Methods 2009, 6:363-369.