Manipulating the pH response of 2,3-diaminopropionic acid rich peptides to mediate highly effective gene silencing with low-toxicity

Journal of Controlled Release

Volumn 172, Issue 3, 2013, Pages 929-938

  Abbate, Vincenzo ^a   Liang, Wanling ^b   Patel, Jayneil ^a   Lan, Yun ^b   Capriotti, Luigi ^a   Iacobucci, Valentina ^a   Bui, Tam T ^a   Chaudhuri, Poulami ^a   Kudsiova, Laila ^a   Vermeer, Louic S ^a   Chan, Patrick F L ^b   Kong, Xiaole ^a   Drake, Alex F ^a   Lam, Jenny K W ^b   Bansal, Sukhvinder S ^a   Mason, A James ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Endocytosis; Manipulation of pH response; Monocytes; pH responsive peptides; siRNA delivery

Indexed keywords

ENDOCYTOSIS; MONOCYTES; PH RESPONSE; PH-RESPONSIVE PEPTIDES; SIRNA DELIVERY;

BODY FLUIDS; CELL CULTURE; CHAINS; ENDOTHELIAL CELLS; GENETIC ENGINEERING; HYDROGEN BONDS; MOLECULAR BIOLOGY; NUCLEIC ACIDS; PH SENSORS; TOXICITY;

PEPTIDES;

2,3 DIAMINOPROPIONIC ACID;

ACYLATION; ARTICLE; BREAST CANCER; CANCER CELL; CELL VIABILITY; CYTOTOXICITY; EPITHELIUM BASAL CELL; GENE SILENCING; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; NUCLEIC ACID TRANSPORT; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN METHYLATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ENDOCYTOSIS; MANIPULATION OF PH RESPONSE; MONOCYTES; PH RESPONSIVE PEPTIDES; SIRNA DELIVERY;

AMINO ACID SEQUENCE; BETA-ALANINE; CELL LINE; CELL LINE, TUMOR; DELAYED-ACTION PREPARATIONS; ENDOCYTOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84887132747     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.09.033     Document Type: Article

References (38)

1. H. Ledford Drug giants turn their backs on RNA interference Nature 468 2010 487
2. S.D. Li, and L. Huang Gene therapy progress and prospects: non-viral gene therapy by systemic delivery Gene Ther. 13 2006 1313 1319 (Pubitemid 44323687)
3. K. Singha, R. Namgung, and W.J. Kim Polymers in small-interfering RNA delivery Nucleic Acid Ther. 21 2011 133 147
4. J. Hoyer, and I. Neundorf Peptide vectors for the nonviral delivery of nucleic acids Acc. Chem. Res. 45 2012 1048 1056
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 (Pubitemid 36254487)
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. 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
8. J.K.W. Lam, W. Liang, Y. Lan, P. Chaudhuri, M.Y.T. Chow, K. Witt, L. Kudsiova, and A.J. Mason Effective endogenous gene silencing mediated by pH responsive peptides proceeds via multiple pathways J. Control. Release 158 2012 293 303
9. X. Gerard, I. Perrault, S. Hanein, E. Silva, K. Bigot, S. Defoort-Delhemmes, M. Rio, A. Munnich, D. Scherman, D. Kaplan, A. Kichler, and J.-M. Rozet AON-mediated exon skipping restores ciliation in fibroblasts harboring the common Leber congenital amaurosis CEP290 mutation Mol. Ther. Nucleic Acids 1 2012 e29
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 30 2012 784 793
11. 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 (Pubitemid 46671157)
12. 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 (Pubitemid 46283102)
13. 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
14. 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
15. V. Iacobucci, F. Di Giuseppe, T.T. Bui, L.S. Vermeer, J. Patel, D. Scherman, A. Kichler, A.F. Drake, and A.J. Mason Control of pH responsive peptide self-association during endocytosis is required for effective gene transfer Biochim. Biophys. Acta 1818 2012 1332 1341
16. 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 (Pubitemid 47558944)
17. D. Eisenberg, R.M. Weiss, C.T. Terwilliger, and W. Wilcox Hydrophobic moments and protein structure Faraday Symp. Chem. Soc. 17 1982 109 120
18. J.K. Kretsinger, and J.P. Schneider Design and application of basic amino acids displaying enhanced hydrophobicity J. Am. Chem. Soc. 125 2003 7907 7913 (Pubitemid 36782168)
19. S.C. Miller, and T.S. Scanlan oNBS-SPPS: a new method for solid-phase peptide synthesis J. Am. Chem. Soc. 120 1998 2690 2691 (Pubitemid 28191692)
20. E.G. Brown, and J.M. Nuss Alkylation of rink's amide linker on polystyrene resin: a reductive amination approach to modified amine-linkers for the solid phase synthesis of N-substituted amide derivatives Tetrahedron Lett. 38 1997 8457 8460 (Pubitemid 27497084)
21. C.T. Bui, F.A. Rasoul, F. Ercole, Y. Pham, and N.J. Maeji Efficiencies of reductive amination reactions on different solid supports Tetrahedron Lett. 39 1998 9279 9282 (Pubitemid 28539284)
22. D.W. Gordon, and J. Steele Reductive alkylation on a solid phase: synthesis of a piperazinedione combinatorial library Bioorg. Med. Chem. Lett. 5 1995 47 50
23. 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 (Pubitemid 351540911)
24. M. Hoernke, C. Schwieger, A. Kerth, and A. Blume Binding of cationic pentapeptides with modified side chain lengths to negatively charged lipid membranes: complex interplay of electrostatic and hydrophobic interactions Biochim. Biophys. Acta 1818 2012 1663 1672
25. O. Boussif, F. Lezoualc'h, M.A. Zanta, M.D. Mergny, D. Scherman, B. Demeneix, and J.P. Behr A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine Proc. Natl. Acad. Sci. 92 1995 7297 7301
26. J.P. Behr The proton sponge: a trick to enter cells the viruses did not exploit Chim. Int. J. Chem. 51 1997 34 36
27. D.W. Pack, A.S. Hoffman, S. Pun, and P.S. Stayton Design and development of polymers for gene delivery Nat. Rev. Drug Discov. 4 2005 581 593 (Pubitemid 40975711)
28. N.D. Sonawane, F.C. Szoka Jr., and A.S. Verkman Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes J. Biol. Chem. 278 2003 44826 44831 (Pubitemid 37377241)
29. W. Liang, P.C.L. Kwok, M.Y.T. Chow, P. Tang, A.J. Mason, H.-K. Chan, and J.K.W. Lam Formulation of pH responsive peptides as inhalable dry powders for pulmonary delivery of nucleic acids Eur. J. Pharm. Biopharm. 2013 10.1016/j.ejpb.2013.05.006
30. N. Sanders, C. Rudolph, K. Braeckmans, S.C. De Smedt, and J. Demeester Extracellular barriers in respiratory gene therapy Adv. Drug Deliv. Rev. 61 2009 115 127
31. J. Goerke Pulmonary surfactant: functions and molecular composition Biochim. Biophys. Acta 1408 1998 79 89 (Pubitemid 28517859)
32. H.-J. Park, Y. Zhang, S.P. Georgescu, K.L. Johnson, D. Kong, and J.B. Galper Human umbilical vein endothelial cells and human dermal microvascular endothelial cells offer new insights into the relationship between lipid metabolism and angiogenesis Stem Cell Rev. 2 2006 93 102 (Pubitemid 46132376)
33. 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 (Pubitemid 41150132)
34. M.B. Maeß, I. Buers, H. Robenek, and S. Lorkowski Improved protocol for efficient nonviral transfection of premature THP-1 macrophages Cold Spring Harb. Protoc. 2011 10.1101/pdb.prot5612
35. F. Leuschner Therapeutic siRNA silencing in inflammatory monocytes in mice Nat. Biotechnol. 29 2011 1005 1010
36. R.K. Giri, V. Rajagopal, S. Shahi, B.V. Zlokovic, and V.K. Kalra Mechanism of amyloid peptide induced CCR5 expression in monocytes and its inhibition by siRNA for Egr-1 Am. J. Physiol. Cell Physiol. 289 2005 C264 C276
37. I. Theurl, M. Theurl, M. Sifert, S. Mair, M. Nairz, H. Rumpold, H. Zoller, R. Bellmann-Weiler, H. Niederegger, H. Talasz, and G. Weiss Autocrine formation of hepcidin induces iron retention in human monocytes Blood 111 2008 2392 2399 (Pubitemid 351451452)
38. R. Tibes, J.M. Bogenberger, L. Chaudhuri, R.T. Hagelstrom, D. Chow, M.E. Buechel, I.M. Gonzales, T. Demuth, J. Slack, R.A. Mesa, E. Braggio, H.H. Yin, S. Arora, and D.O. Azorsa RNAi screening of the kinome with cytarabine in leukemias Blood 119 2012 2863 2871