Internalization of novel non-viral vector TAT-streptavidin into human cells

BMC Biotechnology

Volumn 7, Issue , 2007, Pages

  Rinne, Johanna ^a   Albarran, Brian ^b   Jylhävä, Juulia ^a   Ihalainen, Teemu O ^a   Kankaanpää, Pasi ^a   Hytönen, Vesa P ^a,c   Stayton, Patrick S ^b   Kulomaa, Markku S ^a,d   Vihinen Ranta, Maija ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b University of Washington   (United States)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF TAMPERE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXICITY; HUMAN CELLS; IMMUNODEFICIENCY; THERAPEUTICS;

CELLS; CYTOLOGY; IMMUNOLOGY; PROTEINS; VIRUSES;

BIOTECHNOLOGY;

CLATHRIN; POLYACRYLIC ACID; STREPTAVIDIN; TRANSACTIVATOR PROTEIN;

ARTICLE; CANCER CELL CULTURE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; NONVIRAL GENE DELIVERY SYSTEM; PINOCYTOSIS; PROTEIN LOCALIZATION; PROTEIN SECRETION;

DRUG DELIVERY SYSTEMS; GENE PRODUCTS, TAT; GENETIC VECTORS; HELA CELLS; HUMANS; PROTEIN ENGINEERING; RECOMBINANT FUSION PROTEINS; STREPTAVIDIN; VIRUSES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33846887854     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-7-1     Document Type: Article

References (50)

1. Jarver P Langel U The use of cell-penetrating peptides as a tool for gene regulation Drug Discov Today 2004 9 395-402 10.1016/ S1359-6446(04)03042-9 15081956
2. Trehin R Merkle HP Chances and pitfalls of cell penetrating peptides for cellular drug delivery Eur J Pharm Biopharm 2004 58 209-223 10.1016/ j.ejpb.2004.02.018 15296950
3. Cao G Pei W Ge H Liang Q Luo Y Sharp FR Lu A Ran R Graham SH Chen J 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 2002 22 5423-5431 12097494
4. Lindsay MA Peptide-mediated cell delivery: Application in protein target validation Curr Opin Pharmacol 2002 2 587-594 10.1016/ S1471-4892(02)00199-6 12324264
5. Vives E Charneau P van Rietschoten J Rochat H Bahraoui E Effects of the Tat basic domain on human immunodeficiency virus type 1 transactivation, using chemically synthesized Tat protein and Tat peptides J Virol 1994 68 3343-3353 236825 8151793
6. Berkhout B Jeang KT Trans activation of human immunodeficiency virus type 1 is sequence specific for both the single-stranded bulge and loop of the trans-acting-responsive hairpin: A quantitative analysis J Virol 1989 63 5501-5504 251225 2479775
7. Hauber J Malim MH Cullen BR Mutational analysis of the conserved basic domain of human immunodeficiency virus tat protein J Virol 1989 63 1181-7 247813 2536828
8. Frankel AD Pabo CO Cellular uptake of the tat protein from human immunodeficiency virus Cell 1988 55 1189-1193 10.1016/ 0092-8674(88)90263-2 2849510
9. Mann DA Frankel AD Endocytosis and targeting of exogenous HIV-1 Tat protein Embo J 1991 10 1733-1739 452844 2050110
10. Albarran B To R Stayton PS A TAT-streptavidin fusion protein directs uptake of biotinylated cargo into mammalian cells Protein Eng Des Sel 2005 18 147-152 10.1093/protein/gzi014 15820981
11. Fawell S Seery J Daikh Y Moore C Chen LL Pepinsky B Barsoum J Tat-mediated delivery of heterologous proteins into cells Proc Natl Acad Sci USA 1994 91 664-668 43009 8290579 10.1073/pnas.91.2.664
12. Schwarze SR Ho A Vocero-Akbani A Dowdy SF In vivo protein transduction: delivery of a biologically active protein into the mouse Science 1999 285 1569-1572 10.1126/science.285.5433.1569 10477521
13. Torchilin VP Levchenko TS Rammohan R Volodina N Papahadjopoulos-Sternberg B D'Souza GG Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes Proc Natl Acad Sci USA 2003 100 1972-1977 149943 12571356 10.1073/pnas.0435906100
14. Torchilin VP Rammohan R Weissig V Levchenko TS 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 USA 2001 98 8786-8791 37513 11438707 10.1073/pnas.151247498
15. Eguchi A Akuta T Okuyama H Senda T Yokoi H Inokuchi H Fujita S Hayakawa T Takeda K Hasegawa M Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells J Biol Chem 2001 276 26204-26210 10.1074/jbc.M010625200 11346640
16. Sandgren S Cheng F Belting M Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans J Biol Chem 2002 277 38877-38883 10.1074/jbc.M205395200 12163493
17. Ignatovich IA Dizhe EB Pavlotskaya AV Akifiev BN Burov SV Orlov SV Perevozchikov AP 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 2003 278 42625-42636 10.1074/ jbc.M301431200 12882958
18. Lewin M Carlesso N Tung CH Tang XW Cory D Scadden DT Weissleder R Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells Nat Biotechnol 2000 18 410-414 10.1038/ 74464 10748521
19. Fittipaldi A Ferrari A Zoppe M Arcangeli C Pellegrini V Beltram F Giacca M Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins J Biol Chem 2003 278 34141-34149 10.1074/jbc.M303045200 12773529
20. Ferrari A Pellegrini V Arcangeli C Fittipaldi A Giacca M Beltram F Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time Mol Ther 2003 8 284-294 10.1016/ S1525-0016(03)00122-9 12907151
21. 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 10.1038/nm996 14770178
22. Richard JP Melikov K Brooks H Prevot P Lebleu B Chernomordik LV Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J Biol Chem 2005
23. Saalik P Elmquist A Hansen M Padari K Saar K Viht K Langel U Pooga M Protein cargo delivery properties of cell-penetrating peptides. A comparative study Bioconjug Chem 2004 15 1246-1253 10.1021/bc049938y 15546190
24. Wilbur DS Stayton PS To R Buhler KR Klumb LA Hamlin DK Stray JE Vessella RL Streptavidin in antibody pretargeting. Comparison of a recombinant streptavidin with two Streptavidin mutant proteins and two commercially available streptavidin proteins Bioconjug Chem 1998 9 100-107 10.1021/ bc970152s 9460552
25. Alon R Bayer EA Wilchek M Cell adhesion to streptavidin via RGD-dependent integrins Eur J Cell Biol 1993 60 1-11 8462588
26. Schechter B Arnon R Colas C Burakova T Wilchek M Renal accumulation of streptavidin: Potential use for targeted therapy to the kidney Kidney Int 1995 47 1327-1335 7637262
27. Rosebrough SF Pharmacokinetics and biodistribution of radiolabeled avidin, streptavidin and biotin Nucl Med Biol 1993 20 663-668 10.1016/ 0969-8051(93)90037-U 8358353
28. Snyers L Zwickl H Blaas D Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis J Virol 2003 77 5360-5369 153964 12692238 10.1128/JVI.77.9.5360-5369.2003
29. Koppelhus U Awasthi SK Zachar V Holst HU Ebbesen P Nielsen PE Cell-dependent differential cellular uptake of PNA, peptides, and PNA-peptide conjugates Antisense Nucleic Acid Drug Dev 2002 12 51-63 10.1089/108729002760070795 12074365
30. Nakase I Niwa M Takeuchi T Sonomura K Kawabata N Koike Y Takehashi M Tanaka S Ueda Simpson JC Cellular uptake of arginine-rich peptides: roles for K macropinocytosis and actin rearrangement Mol Ther 2004 10 1011-1022 10.1016/j.ymthe.2004.08.010 15564133
31. Hailstones D Sleer LS Parton RG Stanley KK Regulation of caveolin and caveolae by cholesterol in MDCK cells J Lipid Res 1998 39 369-379 9507997
32. Fujimoto T Kogo H Nomura R Une T Isoforms of caveolin-1 and caveolar structure J Cell Sci 2000 113 Pt 19 3509-3517 10984441
33. Parton RG Richards AA Lipid rafts and caveolae as portals for endocytosis: New insights and common mechanisms Traffic 2003 4 724-738 10.1034/j.1600-0854.2003.00128.x 14617356
34. Conner SD Schmid SL Regulated portals of entry into the cell Nature 2003 422 37-44 10.1038/nature01451 12621426
35. Daro E van der Sluijs P Galli T Mellman I Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling Proc Natl Acad Sci USA 1996 93 9559-9564 38467 8790369 10.1073/pnas.93.18.9559
36. Kaplan IM Wadia JS Dowdy SF Cationic TAT peptide transduction domain enters cells by macropinocytosis J Control Release 2005 102 247-253 10.1016/j.jconrel.2004.10.018 15653149
37. West A Bretscher M Watts C Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells J Cell Biol 1989 109 2731-2739 10.1083/jcb.109.6.2731 2556406
38. Sampath P Pollard TD Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments Biochemistry 1991 30 1973-1980 10.1021/ bi00221a034 1899622
39. Pujals S Fernandez-Carneado J Lopez-Iglesias C Kogan MJ Giralt E Mechanistic aspects of CPP-mediated intracellular drug delivery: relevance of CPP self-assembly Biochim Biophys Acta 2006 1758 264-279 10.1016/j.bbamem.2006.01.006 16545772
40. Lackey CA Press OW Hoffman AS Stayton PS A biomimetic pH-responsive polymer directs endosomal release and intracellular delivery of an endocytosed antibody complex Bioconjug Chem 2002 13 996-1001 10.1021/ bc010053l 12236781
41. Lackey CA Murthy N Press OW Tirrell DA Hoffman AS Stayton PS Hemolytic activity of pH-responsive polymer-streptavidin bioconjugates Bioconjug Chem 1999 10 401-405 10.1021/bc980109k 10346870
42. Kyriakides TR Cheung CY Murthy N Bornstein P Stayton PS Hoffman AS pH-sensitive polymers that enhance intracellular drug delivery in vivo J Control Release 2002 78 295-303 10.1016/S0168-3659(01)00504-1 11772470
43. Jones RA Cheung CY Black FE Zia JK Stayton PS Hoffman AS Wilson MR Poly(2-alkylacrylic acid) polymers deliver molecules to the cytosol by pH-sensitive disruption of endosomal vesicles Biochem J 2003 372 65-75 1223370 12583812 10.1042/BJ20021945
44. Pepinsky RB Androphy EJ Corina K Brown R Barsoum J Specific inhibition of a human papillomavirus E2 trans-activator by intracellular delivery of its repressor DNA Cell Biol 1994 13 1011-1019 7945933
45. Vocero-Akbani AM Heyden NV Lissy NA Ratner L Dowdy SF Killing HIV-infected cells by transduction with an HIV protease-activated caspase-3 protein Nat Med 1999 5 29-33 10.1038/4710 9883836
46. Tasciotti E Zoppe M Giacca M Transcellular transfer of active HSV-1 thymidine kinase mediated by an 11-amino-acid peptide from HIV-1 Tat Cancer Gene Ther 2003 10 64-74 10.1038/sj.cgt.7700526 12489030
47. Wang HY Fu T Wang G Zeng G Perry-Lalley DM Yang JC Restifo NP Hwu P Wang RF Induction of CD4(+) T cell-dependent antitumor immunity by TAT-mediated tumor antigen delivery into dendritic cells J Clin Invest 2002 109 1463-1470 151000 12045260 10.1172/JCI200215399
48. Gratton JP Yu J Griffith JW Babbitt RW Scotland RS Hickey R Giordano FJ Sessa WC Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo Nat Med 2003 9 357-362 10.1038/nm835 12598894
49. Murthy N Campbell J Fausto N Hoffman AS Stayton PS Bioinspired pH-responsive polymers for the intracellular delivery of biomolecular drugs Bioconjug Chem 2003 14 412-419 10.1021/bc020056d 12643752
50. Bananis E Murray JW Stockert RJ Satir P Wolkoff AW Microtubule and motor-dependent endocytic vesicle sorting in vitro J Cell Biol 2000 151 179-186 10.1083/jcb.151.1.179 11018063