A gene delivery system for human cells mediated by both a cell-penetrating peptide and a piggyBac transposase

Biomaterials

Volumn 32, Issue 26, 2011, Pages 6264-6276

  Lee, Cheng Yi ^a   Li, Jheng Fong ^a   Liou, Ji Sing ^a   Charng, Yuh Chyang ^b   Huang, Yue Wern ^c   Lee, Han Jung ^a  

^a NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c MISSOURI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (United States)

Author keywords

Cell penetrating peptide (CPP); Gene delivery; PiggyBac (PB); Polyarginine; Transposon

Indexed keywords

CELL-PENETRATING PEPTIDE; GENE DELIVERY; PIGGYBAC (PB); POLYARGININE; TRANSPOSON;

AMINO ACIDS; BACTERIOPHAGES; CELL CULTURE; CELLS; DNA; FLUORESCENCE; GENE EXPRESSION; GENE TRANSFER; PEPTIDES;

GENE THERAPY;

AMINO ACID; CELL PENETRATING PEPTIDE; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; POLYARGININE; RED FLUORESCENT PROTEIN; TRANSPOSASE; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CELL LINE; DOWNSTREAM PROCESSING; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE THERAPY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; NONVIRAL GENE DELIVERY SYSTEM; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENICS; TRANSPOSON;

CELL LINE, TUMOR; CELL SURVIVAL; CELL-PENETRATING PEPTIDES; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; TRANSFECTION; TRANSPOSASES;

EUKARYOTA;

EID: 79959899351     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.05.012     Document Type: Article

References (60)

1. McClintock B. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 1950, 36(3):344-355.
2. Jones R.N. McClintock's controlling elements: the full story. Cytogenet Genome Res 2005, 109(1-3):90-103.
3. 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(4):501-510.
4. Wang W., Lin C., Lu D., Ning Z., Cox T., Melvin D., et al. Chromosomal transposition of piggyBac in mouse embryonic stem cells. Proc Natl Acad Sci USA 2008, 105(27):9290-9295.
5. Wu S.C., Meir Y.J., Coates C.J., Handler A.M., Pelczar P., Moisyadi S., et al. piggyBac is a flexible and highly active transposon as compared to Sleeping Beauty, Tol2, and Mos1 in mammalian cells. Proc Natl Acad Sci USA 2006, 103(41):15008-15013.
6. Ding S., Wu X., Li G., Han M., Zhang Y., Xu T. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 2005, 122(3):473-483.
7. Dupuy A.J., Akagi K., Largaespada D.A., Copeland N.G., Jenkins N.A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 2005, 436(7048):221-226.
8. Collier L.S., Carlson C.M., Ravimohan S., Dupuy A.J., Largaespada D.A. Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature 2005, 436(7048):272-276.
9. Cary L.C., Goebel M., Corsaro B.G., Wang H.G., Rosen E., Fraser M.J. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 1989, 172(1):156-169.
10. Wilson M.H., Coates C.J., George A.L. PiggyBac transposon-mediated gene transfer in human cells. Mol Ther 2007, 15(1):139-145.
11. Balu B., Shoue D.A., Fraser M.J., Adams J.H. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc Natl Acad Sci USA 2005, 102(45):16391-16396.
12. Lacoste A., Berenshteyn F., Brivanlou A.H. An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell 2009, 5(3):332-342.
13. Balu B., Chauhan C., Maher S.P., Shoue D.A., Kissinger J.C., Fraser M.J., et al. piggyBac is an effective tool for functional analysis of the Plasmodium falciparum genome. BMC Microbiol 2009, 9:83.
14. Rad R., Rad L., Wang W., Cadinanos J., Vassilious G., Rice S., et al. PiggyBac transposon mutagenesis: a tool for cancer gene discovery in mice. Science 2010, 330(6007):1104-1107.
15. El-Sayed A., Futaki S., Harashima H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J 2009, 11(1):13-22.
16. Raagel H., Saalik P., Pooga M. Peptide-mediated protein delivery-which pathways are penetrable?. Biochim Biophys Acta 2010, 1798(12):2240-2248.
17. Fonseca S.B., Pereira M.P., Kelley S.O. Recent advances in the use of cell-penetrating peptides for medical and biological applications. Adv Drug Deliv Rev 2009, 61(11):953-964.
18. Green M., Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus Tat trans-activator protein. Cell 1988, 55(6):1179-1188.
19. Frankel A.D., Pabo C.O. Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 1988, 55(6):1189-1193.
20. Dowdy S.F., Snyder E.L. Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin Drug Deliv 2005, 2(1):43-51.
21. Dietz G.P., Bahr M. Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 2004, 27(2):85-131.
22. Futaki S. Arginine-rich peptides: potential for intracellular delivery of macromolecules and the mystery of the translocation mechanisms. Int J Pharm 2002, 245(1-2):1-7.
23. Nakase I., Takeuchi T., Tanaka G., Futaki S. Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides. Adv Drug Deliv Rev 2008, 60(4-5):598-607.
24. Chang M., Chou J.C., Lee H.J. Cellular internalization of fluorescent proteins via arginine-rich intracellular delivery peptide in plant cells. Plant Cell Physiol 2005, 46(3):482-488.
25. Liu K., Lee H.J., Leong S.S., Liu C.L., Chou C.J. A bacterial indole-3-acetyl-L-aspartic acid hydrolase inhibits mung bean (Vigna radiata L.) seed germination through arginine-rich intracellular delivery. J Plant Growth Regul 2007, 26(3):278-284.
26. Li J.F., Huang Y., Chen R.L., Lee H.J. Induction of apoptosis by gene transfer of human TRAIL mediated by arginine-rich intracellular delivery peptides. Anticancer Res 2010, 30(6):2193-2202.
27. Hu J.W., Liu B.R., Wu C.Y., Lu S.W., Lee H.J. Protein transport in human cells mediated by covalently and noncovalently conjugated arginine-rich intracellular delivery peptides. Peptides 2009, 30(9):1669-1678.
28. Lu S.W., Hu J.W., Liu B.R., Lee C.Y., Li J.F., Chou J.C., et al. Arginine-rich intracellular delivery peptides synchronously deliver covalently and noncovalently linked proteins into plant cells. J Agricult Food Chem 2010, 58(4):2288-2294.
29. Wang Y.H., Chen C.P., Chan M.H., Chang M., Hou Y.W., Chen H.H., et al. Arginine-rich intracellular delivery peptides noncovalently transport protein into living cells. Biochem Biophys Res Commun 2006, 346(3):758-767.
30. Chang M., Chou J.C., Chen C.P., Liu B.R., Lee H.J. Noncovalent protein transduction in plant cells by macropinocytosis. New Phytol 2007, 174(1):46-56.
31. Hou Y.W., Chan M.H., Hsu H.R., Liu B.R., Chen C.P., Chen H.H., et al. Transdermal delivery of proteins mediated by non-covalently associated arginine-rich intracellular delivery peptides. Exp Dermatol 2007, 16(12):999-1006.
32. Liu B.R., Chou J.C., Lee H.J. Cell membrane diversity in noncovalent protein transduction. J Membr Biol 2008, 222(1):1-15.
33. Wang Y.H., Hou Y.W., Lee H.J. An intracellular delivery method for siRNA by an arginine-rich peptide. J Biochem Biophys Methods 2007, 70(4):579-586.
34. Liu B.R., Li J.F., Lu S.W., Lee H.J., Huang Y.W., Shannon K.B., et al. Cellular internalization of quantum dots noncovalently conjugated with arginine-rich cell-penetrating peptides. J Nanosci Nanotechnol 2010, 10(10):6534-6543.
35. Liu B.R., Huang Y.W., Chiang H.J., Lee H.J. Cell-penetrating peptide-functionized quantum dots for intracellular delivery. J Nanosci Nanotechnol 2010, 10(12):7897-7905.
36. Xu Y., Liu B.R., Chiang H.J., Lee H.J., Shannon K.B., Winiarz J.G., et al. Nona-arginine facilitates delivery of quantum dots into cells via multiple pathways. J Biomed Biotechnol 2010, 2010:948543.
37. Liu B.R., Huang Y.W., Winiarz J.G., Chiang H.J., Lee H.J. Intracellular delivery of quantum dots mediated by a histidine- and arginine-rich HR9 cell-penetrating peptide through the direct membrane translocation mechanism. Biomaterials 2011, 32(13):3520-3537.
38. Chen C.P., Chou J.C., Liu B.R., Chang M., Lee H.J. Transfection and expression of plasmid DNA in plant cells by an arginine-rich intracellular delivery peptide without protoplast preparation. FEBS Lett 2007, 581(9):1891-1897.
39. Torchilin V.P., Levchenko T.S., Rammohan R., Volodinan N., Papahadjopoulos-Sternberg B., D'Souza G.G. Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes. Proc Natl Acad Sci USA 2003, 100(4):1972-1977.
40. Kuciak M., Gabus C., Ivanyi-Nagy R., Semrad K., Storchak R., Chaloin O., et al. The HIV-1 transcriptional activator Tat has potent nucleic acid chaperoning activities in vitro. Nucl Acids Res 2008, 36(10):3389-3400.
41. Ziegler A., Seelig J. High affinity of the cell-penetrating peptide HIV-1 Tat-PTD for DNA. Biochemistry 2007, 46(27):8138-8145.
42. Ohlfest J.R., Lobitz P.D., Perkinson S.G., Largaespada D.A. Integration and long-term expression in xenografted human glioblastoma cells using a plasmid-based transposon system. Mol Ther 2004, 10(2):260-268.
43. Emelyanov A., Gao Y., Naqvi N.I., Parinov S. Trans-kingdom transposition of the maize Dissociation element. Genetics 2006, 174(3):1095-1104.
44. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N.G., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004, 22(12):1567-1572.
45. Cadinanos J., Bradley A. Generation of an inducible and optimized piggyBac transposon system. Nucl Acids Res 2007, 35(12):e87.
46. Chang M., Hsu H.Y., Lee H.J. Dye-free protein molecular weight markers. Electrophoresis 2005, 26(16):3062-3068.
47. Leschziner A.E., Griffin T.J., Grindley N.D. Tn552 transposase catalyzes concerted strand transfer in vitro. Proc Natl Acad Sci USA 1998, 95(13):7345-7350.
48. Claeys Bouuaert C., Chalmers R.M. Gene therapy vectors: the prospects and potentials of the cut-and-paste transposons. Genetica 2009, 138(5):473-484.
49. Gump J.M., Dowdy S.F. Tat transduction: the molecular mechanism and therapeutic prospects. Trends Mol Med 2007, 13(10):443-448.
50. Lobo N.F., Fraser T.S., Adams J.A., Fraser M.J. Interplasmid transposition demonstrates piggyBac mobility in vertebrate species. Genetica 2006, 128(1-3):347-357.
51. Nakanishi H., Higuchi Y., Kawakami S., Yamashita F., Hashida M. piggyBac transposon-mediated long-term gene expression in mice. Mol Ther 2010, 18(4):707-714.
52. Macleod D., Lovell-Badge R., Jones S., Jackson I. A promoter trap in embryonic stem (ES) cells selects for integration of DNA into CpG islands. Nucl Acids Res 1991, 19(1):17-23.
53. Grimm S. The art and design of genetic screens: mammalian culture cells. Nat Rev Genet 2004, 5(3):179-189.
54. Urschitz J., Kawasumi M., Owens J., Morozumi K., Yamashiro H., Stoytchev I., et al. Helper-independent piggyBac plasmids for gene delivery approaches: strategies for avoiding potential genotoxic effects. Proc Natl Acad Sci USA 2010, 107(18):8117-8122.
55. Carison C.M., Frandsen J.L., Kirchhof N., McIvor R.S., Largaespada D.A. Somatic integration of an oncogene-harboring Sleeping Beauty transposon models liver tumor development in the mouse. Proc Natl Acad Sci USA 2005, 102(47):17059-17064.
56. St Johnston D. The art and design of genetic screens: Drosophila melanogaster. Nat Rev Genet 2002, 3(3):176-188.
57. Hayes F. Transposon-based strategies for microbial functional genomics and proteomics. Annu Rev Genet 2003, 37:3-29.
58. Yusa K., Zhou L., Li M.A., Bradley A., Craig N.L. A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci USA 2011, 108(4):1531-1536.
59. Sun L.V., Jin K., Liu Y., Yang W., Xie X., Ye L., et al. PBmice: an integrated database system of piggyBac (PB) insertional mutations and their characterizations in mice. Nucl Acids Res 2007, 36:D729-D734.
60. Kahlig K.M., Saridey S.K., Kaja A., Daniels M.A., George A.L., Wilson M.H. Multiplexed transposon-mediated stable gene transfer in human cells. Proc Natl Acad Sci USA 2010, 107(4):1343-1348.