Engineering cell-permeant FLP recombinase for tightly controlled inducible and reversible overexpression in embryonic stem cells

Stem Cells

Volumn 28, Issue 5, 2010, Pages 894-902

  Patsch, Christoph ^a   Peitz, Michael ^a   Otte, David M ^a   Kesseler, Daniela ^a   Jungverdorben, Johannes ^a   Wunderlich, Frank Thomas ^b   Brüstle, Oliver ^a   Zimmer, Andreas ^a   Edenhofer, Frank ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

CDX2; Human embryonic stem cells; Inducible overexpression; Protein transduction; Site specific recombination

Indexed keywords

BETA GALACTOSIDASE; CRE RECOMBINASE; RECOMBINASE; TETRACYCLINE; TRANSCRIPTION FACTOR CDX2;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; GENE LOCUS; GENE OVEREXPRESSION; GENETIC ENGINEERING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN PURIFICATION; PROTEIN STABILITY; CELL MEMBRANE PERMEABILITY; EMBRYO; FEMALE; FIBROBLAST; GENE CASSETTE; GENE EXPRESSION; GENE INDUCTION; GENETIC RECOMBINATION; TRANSGENE;

ANIMALS; CELL DEDIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL MEMBRANE PERMEABILITY; DNA NUCLEOTIDYLTRANSFERASES; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE PRODUCTS, TAT; GENETIC ENGINEERING; HUMANS; INTEGRASES; MICE; MICE, INBRED C57BL; NIH 3T3 CELLS; RECOMBINANT FUSION PROTEINS; TRANSDUCTION, GENETIC;

EID: 77952377151     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.417     Document Type: Article

References (38)

1. Branda CS, Dymecki SM. Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev Cell 2004;6:7-28.
2. Glaser S, Anastassiadis K, Stewart AF. Current issues in mouse genome engineering. Nat Genet 2005;37:1187-1193. (Pubitemid 41568698)
3. Garcia-Otin AL, Guillou F. Mammalian genome targeting using site-specific recombinases. Front Biosci 2006;11:1108-1136. (Pubitemid 43253464)
4. Turakainen H, Saarimaki-Vire J, Sinjushina N et al. Transposition-based method for the rapid generation of gene-targeting vectors to produce Cre/Flp-modifiable conditional knock-out mice. Plos One 2009;4:e4341.
5. Du ZW, Hu BY, Ayala M et al. Cre recombination-mediated cassette exchange for building versatile transgenic human embryonic stem cells lines. Stem Cells 2009;27:1032-1041.
6. Wallace HA, Marques-Kranc F, Richardson M et al. Manipulating the mouse genome to engineer precise functional syntenic replacements with human sequence. Cell 2007;128:197-209. (Pubitemid 46048892)
7. Yu Y, Bradley A. Engineering chromosomal rearrangements in mice. Nat Rev Genet 2001;2:780-790.
8. Brault V, Pereira P, Duchon A et al. Modeling chromosomes in mouse to explore the function of genes, genomic disorders, and chromosomal organization. Plos Genet 2006;2:e86. (Pubitemid 44147396)
9. Raymond CS, Soriano P. High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. Plos One 2007;2:e162.
10. Ringrose L, Lounnas V, Ehrlich L et al. Comparative kinetic analysis of FLP and cre recombinases: Mathematical models for DNA binding and recombination. J Mol Biol 1998;284:363-384. (Pubitemid 28542460)
11. Schaft J, Ashery-Padan R, van der Hoeven F et al. Efficient FLP recombination in mouse ES cells and oocytes. Genesis 2001;31:6-10. (Pubitemid 32927793)
12. Andreas S, Schwenk F, Kuter-Luks B et al. Enhanced efficiency through nuclear localization signal fusion on phage PhiC31-integrase: Activity comparison with Cre and FLPe recombinase in mammalian cells. Nucleic Acids Res 2002;30:2299-2306. (Pubitemid 34618980)
13. Nakano M, Odaka K, Ishimura M et al. Efficient gene activation in cultured mammalian cells mediated by FLP recombinase-expressing recombinant adenovirus. Nucleic Acids Res 2001;29:E40.
14. Buchholz F, Angrand PO, Stewart AF. A simple assay to determine the functionality of Cre or FLP recombination targets in genomic manipulation constructs. Nucleic Acids Res 1996;24:3118-3119. (Pubitemid 26289610)
15. Buchholz F, Angrand PO, Stewart AF. Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat Biotechnol 1998; 16:657-662. (Pubitemid 28334324)
16. Edenhofer F. Protein transduction revisited: Novel insights into the mechanism underlying intracellular delivery of proteins. Curr Pharm Des 2008;14:3628-3636.
17. Gump JM, Dowdy SF. TAT transduction: The molecular mechanism and therapeutic prospects. Trends Mol Med 2007;13:443-448.
18. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004;10:310-315.
19. Caron NJ, Quenneville SP, Tremblay JP. Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem Biophys Res Commun 2004;319:12-20.
20. Toniatti C, Bujard H, Cortese R et al. Gene therapy progress and prospects: Transcription regulatory systems. Gene Ther 2004;11:649-657. (Pubitemid 38519272)
21. 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. (Pubitemid 36790260)
22. Zhou BY, Ye Z, Chen G et al. Inducible and reversible transgene expression in human stem cells after efficient and stable gene transfer. Stem Cells 2007;25:779-789. (Pubitemid 46354238)
23. Peitz M, Pfannkuche K, Rajewsky K et al. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: A tool for efficient genetic engineering of mammalian genomes. Proc Natl Acad Sci USA 2002;99:4489-4494. (Pubitemid 34286012)
24. Roberts RM, Ezashi T, Das P. Trophoblast gene expression: Transcription factors in the specification of early trophoblast. Reprod Biol Endocrinol 2004;2:47. (Pubitemid 39130532)
25. Rossant J. Stem cells and early lineage development. Cell 2008;132: 527-531. (Pubitemid 351253691)
26. Patsch C, Edenhofer F. Conditional mutagenesis by cell-permeable proteins: Potential, limitations and prospects. Handb Exp Pharmacol 2007:203-232.
27. Peitz M, Jager R, Patsch C et al. Enhanced purification of cell-permeant Cre and germline transmission after transduction into mouse embryonic stem cells. Genesis 2007;45:508-517. (Pubitemid 47584209)
28. Buch T, Heppner FL, Tertilt C et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods 2005;2:419-426. (Pubitemid 40916560)
29. Iwakoshi NN, Lee AH, Vallabhajosyula P et al. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003;4:321-329. (Pubitemid 36432313)
30. Klotz L, Dani I, Edenhofer F et al. Peroxisome proliferator-activated receptor gamma control of dendritic cell function contributes to development of CD4+ T cell anergy. J Immunol 2007;178:2122-2131. (Pubitemid 46233409)
31. Murakami M, Ichisaka T, Maeda M et al. mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol Cell Biol 2004;24:6710-6718. (Pubitemid 38944350)
32. Xu Y, Liu S, Yu G et al. Excision of selectable genes from transgenic goat cells by a protein transducible TAT-Cre recombinase. Gene 2008;419:70-74.
33. Hadjantonakis AK, Pirity M, Nagy A. Cre recombinase mediated alterations of the mouse genome using embryonic stem cells. Methods Mol Biol 2008;461:111-132.
34. Schmidt-Supprian M, Rajewsky K. Vagaries of conditional gene targeting. Nat Immunol 2007;8:665-668.
35. 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. (Pubitemid 30187435)
36. Tolkunova E, Cavaleri F, Eckardt S et al. The caudal-related protein cdx2 promotes trophoblast differentiation of mouse embryonic stem cells. Stem Cells 2006;24:139-144.
37. Potgens AJ, Gaus G, Frank HG et al. Characterization of trophoblast cell isolations by a modified flow cytometry assay. Placenta 2001;22: 251-255. (Pubitemid 32537044)
38. Xu RH, Chen X, Li DS et al. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 2002;20: 1261-1264. (Pubitemid 35462493)