Control of pH responsive peptide self-association during endocytosis is required for effective gene transfer

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 5, 2012, Pages 1332-1341

  Iacobucci, Valentina ^a   Di Giuseppe, Francesca ^a   Bui, Tam T ^a   Vermeer, Louic S ^a   Patel, Jayneil ^a   Scherman, Daniel ^b   Kichler, Antoine ^b,c   Drake, Alex F ^a   Mason, A James ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Centre National de la Recherche Scientifique   (France)

^c GÉNÉTHON   (France)

Author keywords

Circular dichroism; DNA binding; Endocytosis; Gene delivery; pH responsive peptides

Indexed keywords

DNA; NUCLEIC ACID; SMALL INTERFERING RNA;

ACIDIFICATION; ARTICLE; BINDING AFFINITY; BIOPHYSICS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOCYTOSIS; GENE TARGETING; GENE TRANSFER; HUMAN; HUMAN CELL; LUNG FIBROBLAST; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN RNA BINDING; PROTON TRANSPORT;

CELL LINE, TRANSFORMED; CIRCULAR DICHROISM; DNA; ENDOCYTOSIS; GENE TRANSFER TECHNIQUES; HUMANS; HYDROGEN-ION CONCENTRATION; PEPTIDES; RNA, SMALL INTERFERING;

EID: 84857980289     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.12.018     Document Type: Article

References (40)

1. S.D. Li, and L. Huang Gene therapy progress and prospects: non-viral gene therapy by systemic delivery Gene Ther. 13 2006 1313 1319
2. L. Crombez, M.C. Morris, S. Dufort, G. Aldrian-Herrada, Q. Nguyen, G. McMaster, J.-L. Coll, F. Heitz, and G. Divita Targeting cyclin B1 through peptide-based delivery of siRNA prevents tumour growth Nucleic Acids Res. 37 2006 4559 4569
3. L. Crombez, G. Aldrian-Herrada, K. Konate, Q.N. Nguyen, G.K. McMaster, R. Brasseur, F. Heitz, and G. Divita A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells Mol. Ther. 17 2009 95 103
4. K. Konate, L. Crombez, S. Deshayes, M. Decaffmeyer, A. Thomas, R. Brasseur, G. Aldrian, F. Heitz, and G. Divita Insight into the cellular uptake mechanism of a secondary amphipathic cell-penetrating peptide for siRNA delivery Biochemistry 49 2010 3393 3402
5. A. Kichler, C. Leborgne, J. März, O. Danos, and B. Bechinger Histidine-rich amphipathic peptide antibiotics promote efficient delivery of DNA into mammalian cells Proc. Natl. Acad. Sci. U. S. A. 96 2003 1564 1568
6. A. Kichler, A.J. Mason, and B. Bechinger Cationic amphipathic histidine-rich peptides for gene delivery Biochim. Biophys. Acta 1758 2006 301 307
7. Y. Lan, B. Langlet-Bertin, V. Abbate, L.S. Vermeer, X. Kong, K. Sullivan, C. Leborgne, D. Scherman, R.C. Hider, A.F. Drake, S. Bansal, A. Kichler, and A.J. Mason Incorporation of 2,3-diaminopropionic acid in linear cationic amphipathic peptides produces pH sensitive vectors ChemBioChem 11 2010 1266 1272
8. B. Langlet-Bertin, C. Leborgne, D. Scherman, B. Bechinger, A.J. Mason, and A. Kichler Design and evaluation of histidine-rich amphipathic peptides for siRNA delivery Pharm. Res. 27 2010 1426 1436
9. J.K.W. Lam W. Liang, Y. Lan, P. Chaudhuri, M.Y.T. Chow, K. Witt, L. Kudsiova, A.J. Mason, Effective endogenous gene silencing mediated by pH responsive peptides proceeds via multiple pathways, J. Control. Release (2011), (available online: DOI:10.1016/j.jconrel.2011.11.024)
10. T.T. Zhang, T.H. Kang, B. Ma, Y. Xu, C.-F. Hung, and T.-C. Wu LAH4 enhances CD8 + T cell immunity of protein/peptide-based vaccines Vaccine 2011 10.1016/j.vaccine.2011.11.056
11. P. Midoux, C. Pichon, J.-J. Yaounac, and P.-A. Jaffrès Chemical vectors for gene delivery: a current review on polymers, peptides and lipids containing histidine or imidazole as nucleic acids carriers Br. J. Pharmacol. 157 2009 166 178
12. A.J. Mason, A. Martinez, C. Glaubitz, O. Danos, A. Kichler, and B. Bechinger The antibiotic and DNA transfecting peptide LAH4 selectively associates with, and disorders, anionic lipids in mixed membranes FASEB J. 20 2006 320 322
13. A.J. Mason, C. Leborgne, G. Moulay, A. Martinez, O. Danos, B. Bechinger, and A. Kichler Optimising histidine rich peptides for efficient DNA delivery in the presence of serum J. Control. Release 118 2007 95 104
14. A. Kichler, C. Leborgne, O. Danos, and B. Bechinger Characterisation of the gene transfer process mediated by histidine-rich peptides J. Mol. Med. 85 2007 191 201
15. L. Prongidi-Fix, M. Sugawara, P. Bertani, J. Raya, C. Leborgne, A. Kichler, and B. Bechinger Self-promoted cellular uptake of peptide/DNA transfection complexes Biochemistry 46 2007 11253 11262
16. Y. Lan, Y. Ye, J.K.W. Lam, A.F. Drake, and A.J. Mason Structural contributions to the intracellular targeting strategies of antimicrobial peptides Biochim. Biophys. Acta 1798 2010 1934 1943
17. T.C.B. Vogt, and B. Bechinger The interactions of histidine-containing amphipathic helical peptide antibiotics with lipid bilayers J. Biol. Chem. 274 1999 29115 29121
18. J.H. Davis The description of membrane lipid conformation order and dynamics by 2H-NMR Biochim. Biophys. Acta 737 1983 117 171
19. H. Schäfer, B. Mädler, and F. Volke De-PAKE-ing of NMR powder spectra by nonnegative least- squares analysis with Tikhonov regularization J. Magn. Reson. 116 1995 145 149
20. E. Sternin, M. Bloom, and A.L. MacKay De-PAKE-ing of NMR spectra J. Magn. Reson. 55 1983 274 282
21. A. Seelig, and J. Seelig Dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic-resonance Biochemistry 13 1974 4839 4845
22. S.-T. Yang, J.Y. Lee, H.-J. Kim, Y.-J. Eu, S.Y. Shin, K.-S. Hahm, and J.I. Kim Contribution of a central proline in model amphipathic α-helical peptides to self-association, interaction with phospholipids, and antimicrobial mode of action FEBS J. 2006 4040 4054
23. L.I. Huschtscha, and R.J. Holliday Limited and unlimited growth of SV40-transformed cells from human diploid MRC-5 fibroblasts J. Cell Sci. 63 1983 77 99
24. A.J. Mason Structural determinants of antimicrobial and antiplasmodial activity and selectivity in histidine-rich amphipathic cationic peptides J. Biol. Chem. 284 2009 119 133
25. A. Marquette, A.J. Mason, and B. Bechinger Aggregation and membrane permeabilizing properties of designed histidine-containing cationic linear peptide antibiotics J. Pept. Sci. 14 2008 488 495
26. B. Bechinger Towards membrane protein design: pH-sensitive topology of histidine-containing polypeptides J. Mol. Biol. 263 1996 768 775
27. J. Georgescu, V.H.O. Munhoz, and B. Bechinger NMR structures of the histidine-rich peptide LAH4 in micellar environments: membrane insertion, pH dependent mode of antimicrobial action, and DNA transfection Biophys. J. 99 2010 2507 2515
28. S. McLaughlin The electrostatic properties of membranes Annu. Rev. Biophys. 18 1989 113 136
29. P.K. Glasoe, and F.A. Long Use of glass electrodes to measure acidities in deuterium oxide J. Phys. Chem. 64 1960 188 189
30. R.W. Van Dyke Acidification of lysosomes and endosomes Subcell. Biochem. 27 1996 331 360
31. Y. Chen, M.T. Guarnieri, A.I. Vasil, M.L. Vasil, C.T. Mant, and R.S. Hodges Role of peptide hydrophobicity in the mechanism of action of α-helical antimicrobial peptides Antimicrob. Agents Chemother. 51 2007 1398 1406
32. Z. Wang, and G. Wang APD: the antimicrobial peptide database Nucl. Acids Res. 32 2004 D590 D592
33. S.R. Dennison, M. Whittaker, F. Harris, and D.A. Phoenix Anticancer α-helical peptides and structure/function relationships underpinning their interactions with tumour cell membranes Curr. Prot. Pept. Sci. 7 2006 487 499
34. E. Gonçalves, E. Kitas, and J. Seelig Binding of oligoarginine to membrane lipids and heparan sulfate: structural and thermodynamic characterization of a cell-penetrating peptide Biochemistry 44 2005 2692 2702
35. A. Ziegler Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans Adv. Drug Deliv. Rev. 60 2008 580 597
36. A. Ziegler, and J. Seelig Binding and clustering of glycosaminoglycans: a common property of mono- and multivalent cell-penetrating compounds Biophys. J. 94 2008 2142 2149
37. C.K. Payne, S.A. Jones, C. Chen, and X. Zhuang Internalization and trafficking of cell-surface proteoglycans and proteoglycan-binding ligands Traffic 8 2007 389 401
38. J. Rejman, A. Bragonzi, and M. Conese Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes Mol. Ther. 12 2005 468 474
39. B. Fadnes, Ø. Rekdal, and L. Uhlin-Hansen The anticancer activity of lytic peptides in inhibited by heparan sulphate on the surface of the tumour cells BMC Cancer 9 2009 183
40. B. Fadnes, L. Uhlin-Hansen, I. Lindin, and Ø. Rekdal Small lytic peptides escape the inhibitory effect of heparan sulfate on the surface of cancer cells BMC Cancer 11 2011 116