A novel chimeric cell-penetrating peptide with membrane-disruptive properties for efficient endosomal escape

Journal of Controlled Release

Volumn 163, Issue 3, 2012, Pages 293-303

  Salomone, Fabrizio ^a,b   Cardarelli, Francesco ^b   Di Luca, Mariagrazia ^a   Boccardi, Claudia ^b   Nifosì, Riccardo ^a   Bardi, Giuseppe ^b   Di Bari, Lorenzo ^c   Serresi, Michela ^b   Beltram, Fabio ^a,b  

^a CNR   (Italy)

^b CENTER FOR NANOTECHNOLOGY INNOVATION NEST   (Italy)

^c UNIVERSITY OF PISA   (Italy)

Author keywords

AMP; Chimera; CPP; Delivery; Endocytosis; Escaping

Indexed keywords

AMP; CHIMERA; CPP; DELIVERY; ENDOCYTOSIS; ESCAPING;

AMINO ACIDS; CELLS; CYTOLOGY; ENZYME ACTIVITY; MEMBRANES; MOLECULAR BIOLOGY; MOLECULES; PEPTIDES; POLYPEPTIDES;

CELL ENGINEERING;

CALCEIN; CECROPIN A; CELL PENETRATING PEPTIDE; DEXTRAN; HYBRID PROTEIN; MELITTIN; PEPTIDE DERIVATIVE; PLASMID DNA; POLYPEPTIDE ANTIBIOTIC AGENT; TRANSACTIVATOR PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG DEGRADATION; DRUG DESIGN; DRUG PENETRATION; DRUG STABILITY; DRUG UPTAKE; ENDOCYTOSIS; ENDOSOME; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; CHO CELLS; CRICETINAE; CRICETULUS; DEXTRANS; DNA; ENDOCYTOSIS; ENDOSOMES; FLUORESCEINS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; STAPHYLOCOCCUS AUREUS; TRANSFECTION;

EID: 84867380046     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.09.019     Document Type: Article

References (47)

1. R. Brasseur, and G. Divita Happy birthday cell penetrating peptides: already 20 years Biochim. Biophys. Acta 1798 2010 2177 2181
2. F. Heitz, M.C. Morris, and G. Divita Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics Br. J. Pharmacol. 157 2009 195 206
3. H. Brooks, B. Lebleu, and E. Vives Tat peptide-mediated cellular delivery: back to basics Adv. Drug Deliv. Rev. 57 2005 559 577 (Pubitemid 40255561)
4. P. Lundin, H. Johansson, P. Guterstam, T. Holm, M. Hansen, U. Langel, and S. E.L. Andaloussi Distinct uptake routes of cell-penetrating peptide conjugates Bioconjug. Chem. 19 2008 2535 2542
5. J.S. Wadia, R.V. Stan, and S.F. Dowdy Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat. Med. 10 2004 310 315 (Pubitemid 38667624)
6. J.P. Richard, K. Melikov, H. Brooks, P. Prevot, B. Lebleu, and L.V. Chernomordik Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J. Biol. Chem. 280 2005 15300 15306 (Pubitemid 40562886)
7. A. Ferrari, V. Pellegrini, C. Arcangeli, A. Fittipaldi, M. Giacca, and F. Beltram Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time Mol. Ther. 8 2003 284 294 (Pubitemid 37062838)
8. H. Raagel, P. Saalik, M. Hansen, U. Langel, and M. Pooga CPP-protein constructs induce a population of non-acidic vesicles during trafficking through endo-lysosomal pathway J. Control. Release 139 2009 108 117
9. F. Duchardt, M. Fotin-Mleczek, H. Schwarz, R. Fischer, and R. Brock A comprehensive model for the cellular uptake of cationic cell-penetrating peptides Traffic 8 2007 848 866 (Pubitemid 46971632)
10. A. El-Sayed, S. Futaki, and H. Harashima Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment AAPS J. 11 2009 13 22
11. J.J. Skehel, K. Cross, D. Steinhauer, and D.C. Wiley Influenza fusion peptides Biochem. Soc. Trans. 29 2001 623 626 (Pubitemid 32783669)
12. I.M. Kaplan, J.S. Wadia, and S.F. Dowdy Cationic TAT peptide transduction domain enters cells by macropinocytosis J. Control. Release 102 2005 247 253 (Pubitemid 40093789)
13. E.K. Esbjorner, K. Oglecka, P. Lincoln, A. Graslund, and B. Norden Membrane binding of pH-sensitive influenza fusion peptides. positioning, configuration, and induced leakage in a lipid vesicle model Biochemistry 46 2007 13490 13504 (Pubitemid 350209946)
14. T. Yoshikawa, T. Sugita, Y. Mukai, N. Yamanada, K. Nagano, H. Nabeshi, Y. Yoshioka, S. Nakagawa, Y. Abe, H. Kamada, S. Tsunoda, and Y. Tsutsumi Organelle-targeted delivery of biological macromolecules using the protein transduction domain: potential applications for peptide aptamer delivery into the nucleus J. Mol. Biol. 380 2008 777 782
15. H. Michiue, K. Tomizawa, F.Y. Wei, M. Matsushita, Y.F. Lu, T. Ichikawa, T. Tamiya, I. Date, and H. Matsui The NH2 terminus of influenza virus hemagglutinin-2 subunit peptides enhances the antitumor potency of polyarginine-mediated p53 protein transduction J. Biol. Chem. 280 2005 8285 8289 (Pubitemid 40349730)
16. N. Ohmori, T. Niidome, A. Wada, T. Hirayama, T. Hatakeyama, and H. Aoyagi The enhancing effect of anionic alpha-helical peptide on cationic peptide-mediating transfection systems Biochem. Biophys. Res. Commun. 235 1997 726 729 (Pubitemid 27326552)
17. S.L. Lo, and S. Wang An endosomolytic Tat peptide produced by incorporation of histidine and cysteine residues as a nonviral vector for DNA transfection Biomaterials 29 2008 2408 2414
18. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395 (Pubitemid 34100944)
19. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250 (Pubitemid 40298223)
20. H. Sato, and J.B. Feix Peptide-membrane interactions and mechanisms of membrane destruction by amphipathic alpha-helical antimicrobial peptides Biochim. Biophys. Acta 1758 2006 1245 1256 (Pubitemid 44444829)
21. S. Sandgren, A. Wittrup, F. Cheng, M. Jonsson, E. Eklund, S. Busch, and M. Belting The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis J. Biol. Chem. 279 2004 17951 17956 (Pubitemid 38568102)
22. D.B. Rozema, K. Ekena, D.L. Lewis, A.G. Loomis, and J.A. Wolff Endosomolysis by masking of a membrane-active agent (EMMA) for cytoplasmic release of macromolecules Bioconjug. Chem. 14 2003 51 57 (Pubitemid 36169016)
23. M.L. Mangoni, G. Maisetta, M. Di Luca, L.M. Gaddi, S. Esin, W. Florio, F.L. Brancatisano, D. Barra, M. Campa, and G. Batoni Comparative analysis of the bactericidal activities of amphibian peptide analogues against multidrug-resistant nosocomial bacterial strains Antimicrob. Agents Chemother. 52 2008 85 91
24. Y. Duan, C. Wu, S. Chowdhury, M.C. Lee, G. Xiong, W. Zhang, R. Yang, P. Cieplak, R. Luo, T. Lee, J. Caldwell, J. Wang, and P. Kollman A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24 2003 1999 2012
25. D.A. Case, T.A. Darden, I. Cheatham, C.L. Simmerling, J. Wang, R.E. Duke, R. Luo, R.C. Walker, W. Zhang, K.M. Merz, B.P. Roberts, B. Wang, S. Hayik, A. Roitberg, G. Seabra, I. Kolossvary, K.F. Wong, F. Paesani, J. Vanicek, J. Liu, X. Wu, S.R. Broze, and P.A. Kollman AMBER 11 2010 University of California San Francisco
26. F.Y. Dupradeau, A. Pigache, T. Zaffran, C. Savineau, R. Lelong, N. Grivel, D. Lelong, W. Rosanski, and P. Cieplak The R.E.D. tools: advances in RESP and ESP charge derivation and force field library building Phys. Chem. Chem. Phys. 12 2010 7821 7839
27. A. Mitsutake, Y. Sugita, and Y. Okamoto Generalized-ensemble algorithms for molecular simulations of biopolymers Biopolymers 60 2001 96 123 (Pubitemid 32743528)
28. M. Serresi, R. Bizzarri, F. Cardarelli, and F. Beltram Real-time measurement of endosomal acidification by a novel genetically encoded biosensor Anal. Bioanal. Chem. 393 2009 1123 1133
29. F. Cardarelli, M. Serresi, R. Bizzarri, M. Giacca, and F. Beltram In vivo study of HIV-1 Tat arginine-rich motif unveils its transport properties Mol. Ther. 15 2007 1313 1322 (Pubitemid 46965328)
30. F. Cardarelli, D. Pozzi, A. Bifone, C. Marchini, and G. Caracciolo Cholesterol-dependent macropinocytosis and endosomal escape control the transfection efficiency of lipoplexes in CHO living cells Mol. Pharm. 9 2012 334 340
31. S. Yamano, J. Dai, C. Yuvienco, S. Khapli, A.M. Moursi, and J.K. Montclare Modified Tat peptide with cationic lipids enhances gene transfection efficiency via temperature-dependent and caveolae-mediated endocytosis J. Control. Release 152 2011 278 285
32. S. Pistolesi, R. Pogni, and J.B. Feix Membrane insertion and bilayer perturbation by antimicrobial peptide CM15 Biophys. J. 93 2007 1651 1660 (Pubitemid 47403306)
33. M. Respondek, T. Madl, C. Gobl, R. Golser, and K. Zangger Mapping the orientation of helices in micelle-bound peptides by paramagnetic relaxation waves J. Am. Chem. Soc. 129 2007 5228 5234 (Pubitemid 46651400)
34. S. Piantavigna, G.A. McCubbin, S. Boehnke, B. Graham, L. Spiccia, and L.L. Martin A mechanistic investigation of cell-penetrating Tat peptides with supported lipid membranes Biochim. Biophys. Acta 1808 2011 1811 1817
35. M. Rusnati, G. Tulipano, C. Urbinati, E. Tanghetti, R. Giuliani, M. Giacca, M. Ciomei, A. Corallini, and M. Presta The basic domain in HIV-1 Tat protein as a target for polysulfonated heparin-mimicking extracellular Tat antagonists J. Biol. Chem. 273 1998 16027 16037 (Pubitemid 28311370)
36. T. Sugita, T. Yoshikawa, Y. Mukai, N. Yamanada, S. Imai, K. Nagano, Y. Yoshida, H. Shibata, Y. Yoshioka, S. Nakagawa, H. Kamada, S.I. Tsunoda, and Y. Tsutsumi Comparative study on transduction and toxicity of protein transduction domains Br. J. Pharmacol. 153 2008 1143 1152 (Pubitemid 351415501)
37. F. Cardarelli, M. Serresi, R. Bizzarri, and F. Beltram Tuning the transport properties of HIV-1 Tat arginine-rich motif in living cells Traffic 9 2008 528 539 (Pubitemid 351351613)
38. F. Cardarelli, M. Serresi, A. Albanese, R. Bizzarri, and F. Beltram Quantitative analysis of Tat peptide binding to import carriers reveals unconventional nuclear transport properties J. Biol. Chem. 286 2011 12292 12299
39. R.A. Jones, C.Y. Cheung, F.E. Black, J.K. Zia, P.S. Stayton, A.S. Hoffman, and M.R. Wilson Poly(2-alkylacrylic acid) polymers deliver molecules to the cytosol by pH-sensitive disruption of endosomal vesicles Biochem. J. 372 2003 65 75 (Pubitemid 36609607)
40. D.F. Wallach, and T.L. Steck Fluorescence techniques in microdetermination of metals in biological materials. II. An improved method for direct complexometric titration of calcium in small serum samples Anal. Biochem. 6 1963 176 180
41. Y. Chen, and S.M. Simon In situ biochemical demonstration that P-glycoprotein is a drug efflux pump with broad specificity J. Cell Biol. 148 2000 863 870
42. S.M. Ellerbroek, K. Wennerberg, W.T. Arthur, J.M. Dunty, D.R. Bowman, K.A. DeMali, C. Der, and K. Burridge SGEF, a RhoG guanine nucleotide exchange factor that stimulates macropinocytosis Mol. Biol. Cell 15 2004 3309 3319 (Pubitemid 38850125)
43. J.K. Armstrong, R.B. Wenby, H.J. Meiselman, and T.C. Fisher The hydrodynamic radii of macromolecules and their effect on red blood cell aggregation Biophys. J. 87 2004 4259 4270 (Pubitemid 39602928)
44. P.L. Paine, L.C. Moore, and S.B. Horowitz Nuclear envelope permeability Nature 254 1975 109 114
45. O. Meier, K. Boucke, S.V. Hammer, S. Keller, R.P. Stidwill, S. Hemmi, and U.F. Greber Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake J. Cell Biol. 158 2002 1119 1131
46. E. Henderson, P.G. Haydon, and D.S. Sakaguchi Actin filament dynamics in living glial cells imaged by atomic force microscopy Science 257 1992 1944 1946
47. Y. Shai Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides Biochim. Biophys. Acta 1462 1999 55 70