A protein transduction domain with cell uptake and selectivity profiles that are controlled by multivalency effects

Chemistry and Biology

Volumn 20, Issue 3, 2013, Pages 434-444

  Deporter, Sandra M ^a   Lui, Irene ^a   Mohan, Utpal ^a   McNaughton, Brian R ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHALASIN D; GLYCOSAMINOGLYCAN; HEPARIN; HYBRID PROTEIN; PENETRATIN;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE M13; BLOOD; CAVEOLA; CELL LYSATE; CELL PERMEABILIZATION; CELL STRAIN LNCAP; CELL SURFACE; CELL VIABILITY; ENDOCYTOSIS; ENDOSOME; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS CELL; LUNG FIBROBLAST; MAMMAL CELL; PHAGE DISPLAY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DOMAIN; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; TARGET CELL;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; DRUG DISCOVERY; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; OLIGOPEPTIDES; PEPTIDE LIBRARY; PROTEIN TRANSPORT; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

MAMMALIA;

EID: 84875425464     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.01.015     Document Type: Article

References (58)

1. E. Boisselier, and D. Astruc Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity Chem. Soc. Rev. 38 2009 1759 1782
2. D.G. Bostwick, A. Pacelli, M. Blute, P. Roche, and G.P. Murphy Prostate specific membrane antigen expression in prostatic intraepithelial neoplasia and adenocarcinoma: a study of 184 cases Cancer 82 1998 2256 2261
3. J.J. Cronican, D.B. Thompson, K.T. Beier, B.R. McNaughton, C.L. Cepko, and D.R. Liu Potent delivery of functional proteins into mammalian cells in vitro and in vivo using a supercharged protein ACS Chem. Biol. 5 2010 747 752
4. J.J. Cronican, K.T. Beier, T.N. Davis, J.C. Tseng, W.D. Li, D.B. Thompson, A.F. Shih, E.M. May, C.L. Cepko, and A.L. Kung A class of human proteins that deliver functional proteins into mammalian cells in vitro and in vivo Chem. Biol. 18 2011 833 838
5. J.P. Dassie, X.Y. Liu, G.S. Thomas, R.M. Whitaker, K.W. Thiel, K.R. Stockdale, D.K. Meyerholz, A.P. McCaffrey, J.O. McNamara 2nd, and P.H. Giangrande Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors Nat. Biotechnol. 27 2009 839 849
6. C. De Coupade, A. Fittipaldi, V. Chagnas, M. Michel, S. Carlier, E. Tasciotti, A. Darmon, D. Ravel, J. Kearsey, M. Giacca, and F. Cailler Novel human-derived cell-penetrating peptides for specific subcellular delivery of therapeutic biomolecules Biochem. J. 390 2005 407 418
7. D. Derossi, A.H. Joliot, G. Chassaing, and A. Prochiantz The third helix of the Antennapedia homeodomain translocates through biological membranes J. Biol. Chem. 269 1994 10444 10450
8. S. Deshayes, M.C. Morris, G. Divita, and F. Heitz Cell-penetrating peptides: tools for intracellular delivery of therapeutics Cell. Mol. Life Sci. 62 2005 1839 1849
9. E.A. Dubikovskaya, S.H. Thorne, T.H. Pillow, C.H. Contag, and P.A. Wender Overcoming multidrug resistance of small-molecule therapeutics through conjugation with releasable octaarginine transporters Proc. Natl. Acad. Sci. USA 105 2008 12128 12133
10. G.S. Filonov, K.D. Piatkevich, L.M. Ting, J.H. Zhang, K. Kim, and V.V. Verkhusha Bright and stable near-infrared fluorescent protein for in vivo imaging Nat. Biotechnol. 29 2011 757 761
11. K.G. Ford, B.E. Souberbielle, D. Darling, and F. Farzaneh Protein transduction: an alternative to genetic intervention? Gene Ther. 8 2001 1 4
12. A.D. Frankel, and C.O. Pabo Cellular uptake of the tat protein from human immunodeficiency virus Cell 55 1988 1189 1193
13. S.M. Fuchs, and R.T. Raines Polyarginine as a multifunctional fusion tag Protein Sci. 14 2005 1538 1544
14. C.A. Gabel, and S.A. Foster Mannose 6-phosphate receptor-mediated endocytosis of acid hydrolases: internalization of beta-glucuronidase is accompanied by a limited dephosphorylation J. Cell Biol. 103 1986 1817 1827
15. C. Gao, S. Mao, H.J. Ditzel, L. Farnaes, P. Wirsching, R.A. Lerner, and K.D. Janda A cell-penetrating peptide from a novel pVII-pIX phage-displayed random peptide library Bioorg. Med. Chem. 10 2002 4057 4065
16. A. Ghosh, X. Wang, E. Klein, and W.D.W. Heston Novel role of prostate-specific membrane antigen in suppressing prostate cancer invasiveness Cancer Res. 65 2005 727 731
17. D. Ghosh, Y. Lee, S. Thomas, A.G. Kohli, D.S. Yun, A.M. Belcher, and K.A. Kelly M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer Nat. Nanotechnol. 7 2012 677 682
18. M. Green, and P.M. Loewenstein Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein Cell 55 1988 1179 1188
19. G. Gregoriadis Engineering liposomes for drug delivery: progress and problems Trends Biotechnol. 13 1995 527 537
20. M. Han, V.A. Kickhoefer, G.R. Nemerow, and L.H. Rome Targeted vault nanoparticles engineered with an endosomolytic peptide deliver biomolecules to the cytoplasm ACS Nano 5 2011 6128 6137
21. B.P. Head, H.H. Patel, D.M. Roth, F. Murray, J.S. Swaney, I.R. Niesman, M.G. Farquhar, and P.A. Insel Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components J. Biol. Chem. 281 2006 26391 26399
22. M.D. Henry, S.H. Wen, M.D. Silva, S. Chandra, M. Milton, and P.J. Worland A prostate-specific membrane antigen-targeted monoclonal antibody- chemotherapeutic conjugate designed for the treatment of prostate cancer Cancer Res. 64 2004 7995 8001
23. B. Hughes Antibody-drug conjugates for cancer: poised to deliver? Nat. Rev. Drug Discov. 9 2010 665 667
24. R.S. Israeli, C.T. Powell, J.G. Corr, W.R. Fair, and W.D. Heston Expression of the prostate-specific membrane antigen Cancer Res. 54 1994 1807 1811
25. V. Ivanenkov, F. Felici, and A.G. Menon Uptake and intracellular fate of phage display vectors in mammalian cells Biochim. Biophys. Acta 1448 1999 450 462
26. Y. Kim, A.M. Lillo, S.C. Steiniger, Y. Liu, C. Ballatore, A. Anichini, R. Mortarini, G.F. Kaufmann, B. Zhou, B. Felding-Habermann, and K.D. Janda Targeting heat shock proteins on cancer cells: selection, characterization, and cell-penetrating properties of a peptidic GRP78 ligand Biochemistry 45 2006 9434 9444
27. R.G. Lapidus, C.W. Tiffany, J.T. Isaacs, and B.S. Slusher Prostate-specific membrane antigen (PSMA) enzyme activity is elevated in prostate cancer cells Prostate 45 2000 350 354
28. B. Leader, Q.J. Baca, and D.E. Golan Protein therapeutics: a summary and pharmacological classification Nat. Rev. Drug Discov. 7 2008 21 39
29. S.Z. Li, M.J. McGuire, M. Lin, Y.H. Liu, T. Oyama, X.K. Sun, and K.C. Brown Synthesis and characterization of a high-affinity alphavbeta6-specific ligand for in vitro and in vivo applications Mol. Cancer Ther. 8 2009 1239 1249
30. P. Lundberg, S. El-Andaloussi, T. Sütlü, H. Johansson, and U. Langel Delivery of short interfering RNA using endosomolytic cell-penetrating peptides FASEB J. 21 2007 2664 2671
31. M. Mäe, and U. Langel Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery Curr. Opin. Pharmacol. 6 2006 509 514
32. M. Mammen, S.K. Choi, and G.M. Whitesides Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors Angew. Chem. Int. Ed. 37 1998 2755 2794
33. M. Mano, C. Teodósio, A. Paiva, S. Simões, and M.C. Pedroso de Lima On the mechanisms of the internalization of S4(13)-PV cell-penetrating peptide Biochem. J. 390 2005 603 612
34. J.A. May, H. Ratan, J.R. Glenn, W. Lösche, P. Spangenberg, and S. Heptinstall GPIIb-IIIa antagonists cause rapid disaggregation of platelets pre-treated with cytochalasin D. Evidence that the stability of platelet aggregates depends on normal cytoskeletal assembly Platelets 9 1998 227 232
35. D.P. McGregor Discovering and improving novel peptide therapeutics Curr. Opin. Pharmacol. 8 2008 616 619
36. B.R. McNaughton, J.J. Cronican, D.B. Thompson, and D.R. Liu Mammalian cell penetration, siRNA transfection, and DNA transfection by supercharged proteins Proc. Natl. Acad. Sci. USA 106 2009 6111 6116
37. B.R. Meade, and S.F. Dowdy Enhancing the cellular uptake of siRNA duplexes following noncovalent packaging with protein transduction domain peptides Adv. Drug Deliv. Rev. 60 2008 530 536
38. M. Meyer, A. Philipp, R. Oskuee, C. Schmidt, and E. Wagner Breathing life into polycations: functionalization with pH-responsive endosomolytic peptides and polyethylene glycol enables siRNA delivery J. Am. Chem. Soc. 130 2008 3272 3273
39. J.A. Moss, A. Lillo, Y.S. Kim, C.S. Gao, H. Ditzel, and K.D. Janda A dimerization "switch" in the internalization mechanism of a cell-penetrating peptide J. Am. Chem. Soc. 127 2005 538 539
40. G.P. Murphy, A.A.A. Elgamal, S.L. Su, D.G. Bostwick, and E.H. Holmes Current evaluation of the tissue localization and diagnostic utility of prostate specific membrane antigen Cancer 83 1998 2259 2269
41. D.M. Nanus, M.I. Milowsky, L. Kostakoglu, P.M. Smith-Jones, S. Vallabahajosula, S.J. Goldsmith, and N.H. Bander Clinical use of monoclonal antibody HuJ591 therapy: targeting prostate specific membrane antigen J. Urol. 170 2003 S84 S88 discussion S88-S89
42. T. Nomura, M. Kawamura, H. Shibata, Y. Abe, A. Ohkawa, Y. Mukai, T. Sugita, S. Imai, K. Nagano, and T. Okamoto Creation of a novel cell penetrating peptide, using a random 18mer peptides library Pharmazie 62 2007 569 573
43. M. Oishi, H. Hayashi, K. Itaka, K. Kataoka, and Y. Nagasaki pH-responsive PEGylated nanogels as targetable and low invasive endosomolytic agents to induce the enhanced transfection efficiency of nonviral gene vectors Colloid Polym. Sci. 285 2007 1055 1060
44. A.K. Patri, A. Myc, J. Beals, T.P. Thomas, N.H. Bander, and J.R. Baker Jr. Synthesis and in vitro testing of J591 antibody-dendrimer conjugates for targeted prostate cancer therapy Bioconjug. Chem. 15 2004 1174 1181
45. S.M. Pulukuri, C.S. Gondi, S.S. Lakka, A. Jutla, N. Estes, M. Gujrati, and J.S. Rao RNA interference-directed knockdown of urokinase plasminogen activator and urokinase plasminogen activator receptor inhibits prostate cancer cell invasion, survival, and tumorigenicity in vivo J. Biol. Chem. 280 2005 36529 36540
46. S.S. Rizk, A. Luchniak, S. Uysal, C.M. Brawley, R.S. Rock, and A.A. Kossiakoff An engineered substance P variant for receptor-mediated delivery of synthetic antibodies into tumor cells Proc. Natl. Acad. Sci. USA 106 2009 11011 11015
47. J.E. Schnitzer, P. Oh, E. Pinney, and J. Allard Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules J. Cell Biol. 127 1994 1217 1232
48. N.C. Shaner, R.E. Campbell, P.A. Steinbach, B.N.G. Giepmans, A.E. Palmer, and R.Y. Tsien Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein Nat. Biotechnol. 22 2004 1567 1572
49. L. Shen, and J.R. Turner Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis Mol. Biol. Cell 16 2005 3919 3936
50. M. Sung, G.M. Poon, and J. Gariépy The importance of valency in enhancing the import and cell routing potential of protein transduction domain-containing molecules Biochim. Biophys. Acta 1758 2006 355 363
51. D.L.J. Thorek, A.K. Chen, J. Czupryna, and A. Tsourkas Superparamagnetic iron oxide nanoparticle probes for molecular imaging Ann. Biomed. Eng. 34 2006 23 38
52. V.P. Torchilin, and A.N. Lukyanov Peptide and protein drug delivery to and into tumors: challenges and solutions Drug Discov. Today 8 2003 259 266
53. Y.L. Tseng, J.J. Liu, and R.L. Hong Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study Mol. Pharmacol. 62 2002 864 872
54. R.Y. Tsien The green fluorescent protein Annu. Rev. Biochem. 67 1998 509 544
55. L.H. Wang, K.G. Rothberg, and R.G.W. Anderson Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation J. Cell Biol. 123 1993 1107 1117
56. G.L. Wright Jr., C. Haley, M.L. Beckett, and P.F. Schellhammer Expression of prostate-specific membrane antigen in normal, benign, and malignant prostate tissues Urol. Oncol. 1 1995 18 28
57. A.M. Wu, and P.D. Senter Arming antibodies: prospects and challenges for immunoconjugates Nat. Biotechnol. 23 2005 1137 1146
58. O. Zelphati, Y. Wang, S. Kitada, J.C. Reed, P.L. Felgner, and J. Corbeil Intracellular delivery of proteins with a new lipid-mediated delivery system J. Biol. Chem. 276 2001 35103 35110