"soft" calcium crosslinks enable highly efficient gene transfection using TAT peptide

Pharmaceutical Research

Volumn 26, Issue 12, 2009, Pages 2619-2629

  Baoum, Abdulgader ^a   Xie, Sheng Xue ^a   Fakhari, Amir ^b   Berkland, Cory ^a,b  

^a UNIVERSITY OF KANSAS   (United States)

^b University of Kansas   (United States)

Author keywords

A549 cells; Gene delivery; Plasmid DNA; Polyethylenimine; TAT

Indexed keywords

CALCIUM ION; PLASMID DNA; TRANSACTIVATOR PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; DRUG CYTOTOXICITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROTEIN DNA BINDING; TRANSMISSION ELECTRON MICROSCOPY;

CALCIUM; CELL LINE; CROSS-LINKING REAGENTS; ELECTROPHORESIS, AGAR GEL; EPITHELIAL CELLS; GENE TRANSFER TECHNIQUES; GENES, TAT; HUMANS; LUNG; PARTICLE SIZE; PEPTIDES; TRANSFECTION;

EID: 70449094651     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-009-9976-1     Document Type: Article

References (74)

1. E Check 2002 A tragic setback Nature 420 116 8 10.1038/420116a 1:CAS:528:DC%2BD38Xos1Ggurk%3D 12432357 (Pubitemid 35340095)
2. PL Felgner 1997 Nonviral strategies for gene therapy Sci Am 276 102 6 1:CAS:528:DyaK2sXjsFOltbY%3D 9163942
3. MJ Hope B Mui S Ansell QF Ahkong 1998 Cationic lipids, phosphatidylethanolamine and the intracellular delivery of polymeric, nucleic acid-based drugs (Review) Mol Membr Biol 15 1 14 10.3109/09687689809027512 1:CAS:528:DyaK1cXis1Wmsb0%3D 9595549
4. E Marshall 1999 Clinical trials: gene therapy death prompts review of adenovirus vector Science 286 2244 10.1126/science.286.5448.2244 1:CAS:528:DC%2BD3cXjs1Sq 10636774 (Pubitemid 30016842)
5. M Peeters GA Patijn A Lieber L Meuse MA Kay 1996 Adenovirus-mediated hepatic gene transfer in mice: comparison of intravascular and biliary administration Hum Gene Ther 7 1693 9 10.1089/hum.1996.7.14-1693 1:STN:280:DyaK2s%2FktFGluw%3D%3D 8886840
6. M Thomasand AM Klibanov 2003 Non-viral gene therapy: polycation-mediated DNA delivery Appl Microbiol Biotechnol 62 27 34 10.1007/s00253-003-1321-8 (Pubitemid 36836536)
7. S Yei N Mittereder K Tang C O'Sullivan BC Trapnell 1994 Adenovirus-mediated gene transfer for cystic fibrosis: quantitative evaluation of repeated in vivo vector administration to the lung Gene Ther 1 192 200 1:CAS:528:DyaK2cXlvFGmsL4%3D 7584081
8. Huang L, Hung M. and E. Wagner. Nonviral Vectors for Gene Therapy: Academic; 1999.
9. ME Davis 2002 Non-viral gene delivery systems Curr Opin Biotechnol 13 128 31 10.1016/S0958-1669(02)00294-X 1:CAS:528:DC%2BD38Xis1Clt7k%3D 11950563 (Pubitemid 34310371)
10. PL Felgner TR Gadek M Holm R Roman HW Chan M Wenz JP Northrop GM Ringold M Danielsen 1987 Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure Proc Natl Acad Sci 84 7413 7 10.1073/pnas.84.21.7413 1:CAS:528:DyaL1cXjtlSgug%3D%3D 2823261
11. HEJ Hofland D Nagy JJ Liu K Spratt YL Lee O Danos SM Sullivan 1997 In vivo gene transfer by intravenous administration of stable cationic Lipid/DNA complex Pharm Res 14 742 9 10.1023/A:1012146305040 1:CAS:528:DyaK2sXkt1yit7g%3D 9210191 (Pubitemid 27281668)
12. GN Hortobagyi NT Ueno W Xia S Zhang JK Wolf JB Putnam PL Weiden JS Willey M Carey DL Branham 2001 Cationic liposome-mediated E1A gene transfer to human breast and ovarian cancer cells and its biologic effects: a Phase I clinical trial J Clin Oncol 19 3422 1:CAS:528:DC%2BD3MXlvVamsrk%3D 11454891
13. JG Med 2005 Lipid-mediated siRNA delivery down-regulates exogenous gene expression in the mouse brain at picomolar levels J Gene Med 7 198 207 10.1002/jgm.659 (Pubitemid 40348024)
14. M Ogrisand E Wagner 2002 Targeting tumors with non-viral gene delivery systems Drug Discov Today. 7 479 85 10.1016/S1359-6446(02)02243-2 (Pubitemid 34532575)
15. NS Templeton DD Lasic PM Frederik HH Strey DD Roberts GN Pavlakis 1997 Improved DNA: liposome complexes for increased systemic delivery and gene expression Nat Biotechnol 15 647 52 10.1038/nbt0797-647 1:CAS:528: DyaK2sXktlOgsL0%3D 9219267
16. Sambrook J, Russell DW. Introducing cloned gene into cultured mammalian cells. Molecular cloning: A laboratory manual, vol. 16. 3rd ed. Cold Spring Harbor: Cold Spring Harbor Lab; 2001. p. 16.14-9.
17. MX Tang CT Redemann FC Szoka 1996 In vitro gene delivery by degraded polyamidoamine dendrimers Bioconjug Chem 7 703 14 10.1021/bc9600630 1:CAS:528:DyaK28Xms1Cks7Y%3D 8950489 (Pubitemid 27012712)
18. WT Godbey KK Wu AG Mikos 1999 Poly (ethylenimine) and its role in gene delivery J Control Release 60 149 60 10.1016/S0168-3659(99)00090-5 1:CAS:528:DyaK1MXks1Cqu7s%3D 10425321 (Pubitemid 29335941)
19. M Lundberg S Wikström M Johansson 2003 Cell surface adherence and endocytosis of protein transduction domains Molec Ther 8 143 50 10.1016/S1525-0016(03)00135-7 1:CAS:528:DC%2BD3sXkvFGmsrw%3D (Pubitemid 36939305)
20. CH Tungand R Weissleder 2003 Arginine containing peptides as delivery vectors Adv Drug Deliv Rev 55 281 94 10.1016/S0169-409X(02)00183-7 (Pubitemid 36135919)
21. G Cao W Pei H Ge Q Liang Y Luo FR Sharp A Lu R Ran SH Graham J Chen 2002 In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis J Neurosci 22 5423 1:CAS:528:DC%2BD38XltF2msbo%3D 12097494
22. GPH Dietzand M Bdhr 2004 Delivery of bioactive molecules into the cell: the Trojan horse approach Mol Cell Neurosci 27 85 131 10.1016/j.mcn.2004.03.005 (Pubitemid 39370094)
23. B Guptaand VP Torchilin 2006 Transactivating transcriptional activator-mediated drug delivery Expert Opin Drug Deliv 3 177 90 10.1517/17425247.3.2.177 (Pubitemid 43338090)
24. SR Schwarze A Ho A Vocero-Akbani SF Dowdy 1999 In vivo protein transduction: delivery of a biologically active protein into the mouse Science 285 1569 10.1126/science.285.5433.1569 1:CAS:528:DyaK1MXlslOru78%3D 10477521 (Pubitemid 29420581)
25. SR Schwarze KA Hruska SF Dowdy 2000 Protein transduction: unrestricted delivery into all cells? Trends Cell Biol 10 290 5 10.1016/S0962-8924(00)01771-2 1:CAS:528:DC%2BD3cXktlCmsro%3D 10856932 (Pubitemid 30387038)
26. AM Koch F Reynolds HP Merkle R Weissleder L Josephson 2005 Transport of surface-modified nanoparticles through cell monolayers ChemBioChem 6 337 45 10.1002/cbic.200400174 1:CAS:528:DC%2BD2MXhsVKhurc%3D 15651046 (Pubitemid 40879747)
27. D Derossi S Calvet A Trembleau A Brunissen G Chassaing A Prochiantz 1996 Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent J Biol Chem 271 18188 10.1074/jbc.271.30.18188 1:CAS:528:DyaK28XksFyhsLs%3D 8663410 (Pubitemid 26250811)
28. S Deshayes A Heitz MC Morris P Charnet G Divita F Heitz 2004 Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis Biochemistry 43 1449 57 10.1021/bi035682s 1:CAS:528:DC%2BD2cXltFOitw%3D%3D 14769021 (Pubitemid 38200550)
29. ST Henriques J Costa M Castanho 2005 Translocation of β-galactosidase mediated by the cell-penetrating peptide Pep-1 into lipid vesicles and human HeLa cells is driven by membrane electrostatic potential Biochemistry 5 9
30. M Mano C Teodosio A Paiva S Simoes MCP de Lima 2005 On the mechanisms of the internalization of S413-PV cell-penetrating peptide Biochem J 390 603 10.1042/BJ20050577 1:CAS:528:DC%2BD2MXoslKgtbk%3D 15907190 (Pubitemid 41337122)
31. LN Patel JL Zaro WC Shen 2007 Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives Pharm Res 24 1977 92 10.1007/s11095-007-9303-7 1:CAS:528:DC%2BD2sXhtV2msb3K 17443399 (Pubitemid 47493563)
32. E Vives JP Richard C Rispal B Lebleu 2003 TAT peptide internalization: seeking the mechanism of entry Current Protein and Peptide Science 4 125 32 10.2174/1389203033487306 1:CAS:528:DC%2BD3sXitlSrt7g%3D 12678851 (Pubitemid 36834011)
33. S Console C Marty C Garcia-Echeverria R Schwendener K Ballmer-Hofer 2003 Antennapedia and HIV transactivator of transcription (TAT) "Protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans J Biol Chem 278 35109 14 10.1074/jbc.M301726200 1:CAS:528:DC%2BD3sXntVWqtL4%3D 12837762 (Pubitemid 37102274)
34. C Foerg U Ziegler J Fernandez-Carneado E Giralt R Rennert AG Beck-Sickinger HP Merkle 2005 Decoding the entry of two novel cell-penetrating peptides in HeLa cells: lipid raft-mediated endocytosis and endosomal escape Biochemistry 44 72 81 10.1021/bi048330+ 1:CAS:528:DC%2BD2cXhtVCrsb3O 15628847 (Pubitemid 40095708)
35. S Gerbal-Chaloin C Gondeau G Aldrian-Herrada F Heitz C Gauthier-Rouviere G Divita 2007 First step of the cell-penetrating peptide mechanism involves Rac1 GTPase-dependent actin-network remodelling Biol Cell 99 223 38 10.1042/BC20060123 1:CAS:528:DC%2BD2sXlsFWgsLc%3D 17233629 (Pubitemid 46567179)
36. AT Jones 2007 Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides J Cell Mol Med 11 670 84 10.1111/j.1582-4934.2007.00062.x 1:CAS:528:DC%2BD2sXhtFSksrbO 17760832 (Pubitemid 47313298)
37. I Nakase A Tadokoro N Kawabata T Takeuchi H Katoh K Hiramoto M Negishi M Nomizu Y Sugiura S Futaki 2007 Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 492 501 10.1021/bi0612824 1:CAS:528:DC%2BD28Xhtlaru7zK 17209559 (Pubitemid 46105438)
38. JP Richard K Melikov H Brooks P Prevot B Lebleu LV Chernomordik 2005 Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J Biol Chem 280 15300 10.1074/jbc.M401604200 1:CAS:528:DC%2BD2MXjtFSltL4%3D 15687490 (Pubitemid 40562886)
39. M Silhol M Tyagi M Giacca B Lebleu E Vives 2002 Different mechanisms for cellular internalization of the HIV-1 Tat-derived cell penetrating peptide and recombinant proteins fused to Tat Eur J Biochem 269 494 501 10.1046/j.0014-2956. 2001.02671.x 1:CAS:528:DC%2BD38XhtVyhurc%3D 11856307 (Pubitemid 34128006)
40. PEG Thorén D Persson P Isakson M Goksor A Onfelt B Nordén 2003 Uptake of analogs of penetratin, Tat (48-60) and oligoarginine in live cells Biochem Biophys Res Commun 307 100 7 10.1016/S0006-291X(03)01135-5 12849987 (Pubitemid 36808542)
41. JS Wadia RV Stan SF Dowdy 2004 Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat Med 10 310 5 10.1038/nm996 1:CAS:528:DC%2BD2cXhs1Wnurg%3D 14770178 (Pubitemid 38667624)
42. P Jarver Ü Langel 2006 Cell-penetrating peptides-a brief introduction BBA-Biomembranes 1758 260 3 10.1016/j.bbamem.2006.02.012 16574060 (Pubitemid 44262272)
43. M Mae H Myrberg Y Jiang H Paves A Valkna Ü Langel 2005 Internalisation of cell-penetrating peptides into tobacco protoplasts BBA-Biomembranes 1669 101 7 10.1016/j.bbamem.2005.01.006 15893512 (Pubitemid 40704727)
44. S Fawell J Seery Y Daikh C Moore LL Chen B Pepinsky J Barsoum 1994 Tat-mediated delivery of heterologous proteins into cells Proc Natl Acad Sci 91 664 8 10.1073/pnas.91.2.664 1:CAS:528:DyaK2cXhslegsbs%3D 8290579
45. AD Frankeland CO Pabo 1988 Cellular uptake of the tat protein from human immunodeficiency virus Cell 55 1189 93 10.1016/0092-8674(88)90263-2 (Pubitemid 19020071)
46. R Truantand BR Cullen 1999 The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct Importin β-dependent nuclear localization signals Mol Cell Biol 19 1210 7
47. E Vives P Brodin B Lebleu 1997 A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus J Biol Chem 272 16010 7 10.1074/jbc.272.25.16010 1:CAS:528: DyaK2sXktFGnsb4%3D 9188504 (Pubitemid 27265584)
48. A Eguchi T Akuta H Okuyama T Senda H Yokoi H Inokuchi S Fujita T Hayakawa K Takeda M Hasegawa 2001 Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells J Biol Chem 276 26204 10 10.1074/jbc.M010625200 1:CAS:528:DC%2BD3MXlsVKnsL0%3D 11346640 (Pubitemid 37412834)
49. VP Torchilin R Rammohan V Weissig TS Levchenko 2001 TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors Proc Natl Acad Sci 98 8786 10.1073/pnas.151247498 1:CAS:528:DC%2BD3MXls1Witbg%3D 11438707 (Pubitemid 32678105)
50. CH Tungand S Stein 2000 Preparation and applications of peptide-oligonucleotide conjugates Bioconjug Chem 11 605 18 10.1021/bc0000334 (Pubitemid 30738209)
51. S Futaki W Ohashi T Suzuki M Niwa S Tanaka K Ueda H Harashima Y Sugiura 2001 Stearylated arginine-rich peptides: a new class of transfection systems Bioconjug Chem 12 1005 11 10.1021/bc015508l 1:CAS:528:DC%2BD3MXnvVWmtrk%3D 11716693 (Pubitemid 33136872)
52. IA Ignatovich EB Dizhe AV Pavlotskaya BN Akifiev SV Burov SV Orlov AP Perevozchikov 2003 Complexes of plasmid DNA with basic domain 47-57 of the HIV-1 Tat protein are transferred to mammalian cells by endocytosis-mediated pathways J Biol Chem 278 42625 36 10.1074/jbc.M301431200 1:CAS:528:DC%2BD3sXot1alsLo%3D 12882958 (Pubitemid 37310536)
53. S Sandgren F Cheng M Belting 2002 Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans J Biol Chem 277 38877 83 10.1074/jbc.M205395200 1:CAS:528:DC%2BD38Xns1Cnur8%3D 12163493 (Pubitemid 35157770)
54. CH Tung S Mueller R Weissleder 2002 Novel branching membrane translocational peptide as gene delivery vector Bioorg Med Chem 10 3609 14 10.1016/S0968-0896(02)00248-1 1:CAS:528:DC%2BD38Xms12ju7g%3D 12213476
55. A Haberland T Knaus SV Zaitsev B Buchberger A Lun H Haller M Böttger 2000 Histone H1-mediated transfection: serum inhibition can be overcome by Ca2+ Ions Pharm Res 17 229 35 10.1023/A:1007581700996 1:CAS:528:DC%2BD3cXitVOqurc%3D 10751040 (Pubitemid 30158374)
56. G Nchinda K Uberla O Zschornig 2002 Characterization of cationic lipid DNA transfection complexes differing in susceptability to serum inhibition BMC Biotechnol 2 12 10.1186/1472-6750-2-12 12113654 (Pubitemid 38846443)
57. O Zelphati LS Uyechi LG Barron FC Szoka 1998 Effect of serum components on the physico-chemical properties of cationic lipid/oligonucleotide complexes and on their interactions with cells Biochim Biophys Acta (BBA)/Lipids Lipid Metab 1390 119 33 10.1016/S0005-2760(97)00169-0 1:CAS:528:DyaK1cXht1WisLs%3D (Pubitemid 28122331)
58. DS Kwon CH Lin S Chen JK Coward CT Walsh JM Bollinger Jr 1997 Dissection of glutathionylspermidine synthetase/amidase from Escherichia coli into autonomously folding and functional synthetase and amidase domains J Biol Chem 272 2429 10.1074/jbc.272.22.14272 1:CAS:528:DyaK2sXotFeiug%3D%3D 8999955 (Pubitemid 27232840)
59. B Abdallah A Hassan C Benoist D Goula JP Behr BA Demeneix 1996 A powerful nonviral vector for in vivo gene transfer into the adult mammalian brain: polyethylenimine Hum Gene Ther 7 1947 54 10.1089/hum.1996.7.16-1947 1:CAS:528:DyaK28XntF2ksr0%3D 8930654
60. O Boussif F Lezoualc'h MA Zanta MD Mergny D Scherman B Demeneix J Behr 1995 A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine Proc Natl Acad Sci 92 7297 301 10.1073/pnas.92.16.7297 1:CAS:528:DyaK2MXntlKmt7s%3D 7638184
61. CY Huang SS Ma S Lee R Radhakrishnan CS Braun S Choosakoonkriang CM Wiethoff BA Lobo CR Middaugh 2002 Enhancements in gene expression by the choice of plasmid DNA formulations containing neutral polymeric excipients J Pharm Sci 91 1371 81 10.1002/jps.10130 1:CAS:528:DC%2BD38XjsFKjsbc%3D 11977113 (Pubitemid 34651199)
62. BA Lobo JA Vetro DM Suich RN Zuckermann CR Middaugh 2003 Structure/function analysis of peptoid/lipitoid: DNA complexes J Pharm Sci 92 1905 18 10.1002/jps.10450 1:CAS:528:DC%2BD3sXntFymtrY%3D 12950008 (Pubitemid 37071822)
63. W Tiyaboonchai J Woiszwillo CR Middaugh 2003 Formulation and characterization of DNA-polyethylenimine-dextran sulfate nanoparticles Eur J Pharm Sci 19 191 202 10.1016/S0928-0987(03)00102-7 1:CAS:528: DC%2BD3sXls1Onu7Y%3D 12885383 (Pubitemid 36918411)
64. CM Wiethoff JG Koe GS Koe CR Middaugh 2004 Compositional effects of cationic lipid/DNA delivery systems on transgene expression in cell culture J Pharm Sci 93 108 23 10.1002/jps.10519 1:CAS:528:DC%2BD2cXjvFWguw%3D%3D 14648641 (Pubitemid 38081819)
65. S Choosakoonkriang BA Lobo GS Koe JG Koe CR Middaugh 2003 Biophysical characterization of PEI/DNA complexes J Pharm Sci 92 1710 22 10.1002/jps.10437 1:CAS:528:DC%2BD3sXmtFekt78%3D 12884257 (Pubitemid 36929690)
66. ML Forrest JT Koerber DW Pack 2003 A degradable polyethylenimine derivative with low toxicity for highly efficient gene delivery Bioconjug Chem 14 934 40 10.1021/bc034014g 1:CAS:528:DC%2BD3sXms1Cjtr8%3D 13129396 (Pubitemid 37152952)
67. MA Lindsay 2002 Peptide-mediated cell delivery: application in protein target validation Curr Opin Pharmacol 2 587 94 10.1016/S1471-4892(02)00199-6 1:CAS:528:DC%2BD38Xnt1Cku7c%3D 12324264
68. EL Snyderand SF Dowdy 2004 Cell penetrating peptides in drug delivery Pharm Res 21 389 93 10.1023/B:PHAM.0000019289.61978.f5 (Pubitemid 38338971)
69. CW Pouton P Lucas BJ Thomas AN Uduehi DA Milroy SH Moss 1998 Polycation-DNA complexes for gene delivery: a comparison of the biopharmaceutical properties of cationic polypeptides and cationic lipids J Control Release 53 289 99 10.1016/S0168-3659(98)00015-7 1:CAS:528: DyaK1cXitVCjsLY%3D 9741937 (Pubitemid 28218712)
70. D Simberg D Danino Y Talmon A Minsky ME Ferrari CJ Wheeler Y Barenholz 2001 Phase behavior, DNA ordering, and size instability of cationic lipoplexes. Relevance to optimal transfection activity J Biol Chem 276 47453 9 10.1074/jbc.M105588200 1:CAS:528:DC%2BD3MXpt1Gmtrw%3D 11564736
71. J Turek C Dubertret G Jaslin K Antonakis D Scherman B Pitard 2000 Formulations which increase the size of lipoplexes prevent serum-associated inhibition of transfection J Gene Med 2 32 40 10.1002/(SICI)1521-2254(200001/02) 2:1<32::AID-JGM78>3.0.CO;2-U 1:CAS:528:DC%2BD3cXjsVektLg%3D 10765503
72. E Wagner M Cotten R Foisner ML Birnstiel 1991 Transferrin-polycation-DNA complexes: the effect of polycations on the structure of the complex and DNA delivery to cells Proc Natl Acad Sci 88 4255 9 10.1073/pnas.88.10.4255 1:CAS:528:DyaK3MXkt1elsrg%3D 2034670
73. I Moret J Esteban Peris VM Guillem M Benet F Revert F Dasi A Crespo SF Alino 2001 Stability of PEI-DNA and DOTAP-DNA complexes: effect of alkaline pH, heparin and serum J Control Release 76 169 81 10.1016/S0168-3659(01)00415-1 1:CAS:528:DC%2BD3MXmt1Gls70%3D 11532322 (Pubitemid 32786894)
74. M Ruponen S Yla-Herttuala A Urtti 1999 Interactions of polymeric and liposomal gene delivery systems with extracellular glycosaminoglycans: physicochemical and transfection studies BBA-Biomembranes 1415 331 41 10.1016/S0005-2736(98)00199-0 1:CAS:528:DyaK1MXivVWgtg%3D%3D 9889391 (Pubitemid 29065298)