The polymorphic nature of membrane-active peptides from biophysical and structural investigations

Current Protein and Peptide Science

Volumn 13, Issue 7, 2012, Pages 602-610

  Bechinger, Burkhard ^a   Aisenbrey, Christopher ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Alamethicin; Cecropin; Hydrophobic mismatch; Membrane topology; Solid state NMR; Supported bilayers

Indexed keywords

ALAMETHICIN; ANTIMICROBIAL CATIONIC PEPTIDE; CATESTATIN; CECROPIN A; CELL PENETRATING PEPTIDE; DYNORPHIN A; HISTIDINE; MAGAININ 2; MEMBRANE ACTIVE PEPTIDE; NUCLEIC ACID; PENETRATIN; PEPTAIBOL; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; BIOPHYSICS; GENETIC TRANSFECTION; HUMAN; NONHUMAN; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL-PENETRATING PEPTIDES; FUNGI; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MAGAININS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTAIBOLS; PROTEIN CONFORMATION; PROTEINS;

EID: 84874890580     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312804142093     Document Type: Review

References (101)

1. Bechinger, B. The structure, dynamics and orientation of antimicrobial peptides in membranes by solid-state NMR spectroscopy. Biochimica. et Biophysica. Acta., 1999, 1462, 157-183.
2. Brogden, K.A. Antimicrobial peptides, pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3, 238-250.
3. Thennarasu, S.; Tan, A.; Penumatchu R.; Shelburne, C.E.; Heyl, D.L. Ramamoorthy A. Antimicrobial and membrane disrupting activities of a peptide derived from the human cathelicidin antimicrobial peptide LL37. Biophys. J., 2010, 98, 248-257.
4. Epand, R.F., Maloy, L.; Ramamoorthy, A.; Epand, R.M. Amphipathic helical cationic antimicrobial peptides promote rapid formation of crystalline States in the presence of phosphatidylglycerol, lipid clustering in anionic membranes. Biophys. J., 2010, 98, 2564-2573.
5. Jean-Francois, F.; Desbat, B.; Dufourc, E.J. Selectivity of cateslytin for fungi, the role of acidic lipid-ergosterol membrane fluidity in antimicrobial action. FASEB J., 2009.
6. Cronier, F.; Patenaude, A.; Gaudreault, R.; Auger, M. Membrane composition modulates the interaction between a new class of antineoplastic agents deriving from aromatic 2-chloroethylureas and lipid bilayers, a solid-state NMR study. Chem. Phys. Lipids, 2007, 146, 125-35.
7. Fernandez, D. I.; Gehman, J.D.; Separovic, F. Membrane interactions of antimicrobial peptides from Australian frogs. Biochim. Biophys. Acta., 2009,1788,1630-8.
8. Ho, S.W.; Jung, D.; Calhoun, J.R.; Lear, J.D.; Okon, M.; Scott, W.R.; Hancock, R.E.; Straus, S.K. Effect of divalent cations on the structure of the antibiotic daptomycin. Eur. Biophys. J., 2008, 37, 421-33.
9. Chekmenev, E.Y.; Jones, S.M.; Nikolayeva, Y.N.; Vollmar, B.S.; Wagner, T.J.; Gor'kov, P.L.; Brey, W.W.; Manion, M.N.; Daugherty, K. C.; Cotton, M. High-field NMR studies of molecular recognition and structure-function relationships in antimicrobial piscidins at the water-lipid bilayer interface. J. Am. Chem. Soc., 2006, 128, 5308-5309.
10. Schwarz, G.; Stankowski, S.; Rizzo, V. Thermodynamic Analysis of Incorporation and Aggregation in a Membrane, Application to the Pore-Forming Peptide Alamethicin. Biochimica. et Biophysica. Acta., 1986, 861,141-51.
11. Sansom MSP. The Biophysics of Peptide Models of Ion Channels. Prog. Biophys. mol. Biol., 1991, 55, 139-235.
12. White, S.H.; Wimley, W. C. Membrane protein folding and stability, Physical principles. Annu. Rev. Biophys. Biomol. Struct., 1999, 28, 319-365.
13. Bechinger, B. Membrane association and pore formation by alphahelical peptides. Adv. Exp. Med. Biol., 2010, 677, 24-30.
14. Wu, Y.; Huang, H.W.; Olah, G.A. Method of oriented circular dichroism. Biophys. J., 1990, 57, 797-806.
15. Bechinger, B.; Sizun, C. Alignment and structural analysis of membrane polypeptides by 15N and 31P solid-state NMR spectroscopy. Concepts Magnet. Res., 2003, 18A, 130-145
16. Huang, H.W.; Wu, Y. Lipid-alamethicin interactions influence alamethicin orientation. Biophys. J., 1991, 60, 1079-1087.
17. Bechinger, B. Towards membrane protein design, pH dependent topology of histidine-containing polypeptides. J. Mol. Biol., 1996, 263, 768-775.
18. Huang, H.W. Molecular mechanism of antimicrobial peptides, The origin of cooperativity. Biochimica. et Biophysica. Acta., 2006, 1758, 1292-1302.
19. Salnikov, E.; Aisenbrey, C.; Vidovic, V.; Bechinger, B. Solid-state NMR approaches to measure topological equilibria and dynamics of membrane polypeptides. Biochim. Biophys. Acta., 2010,1798, 258-265.
20. Leitgeb, B.; Szekeres, A.; Manczinger, L.; Vagvolgyi, C.; Kredics, L. The history of alamethicin, a review of the most extensively studied peptaibol. Chem. Biodivers, 2007, 4, 1027-1051.
21. Bechinger, B. Structure and Functions of Channel-Forming Polypeptides, Magainins, Cecropins, Melittin and Alamethicin. J. Memb. Biol., 1997,156, 197-211.
22. North, C. L.; Barranger-Mathys, M.; Cafiso, D. S. Membrane orientation of the N-terminal segment of alamethicin determined by solid-state 15 N NMR. Biophys. J., 1995, 69, 2392-2397.
23. Bak, M.; Bywater, R. P.; Hohwy, M.; Thomsen, J. K.; Adelhorst, K.; Jakobsen, H. J.; Sorensen, O.W.; Nielsen, N.C. Conformation of alamethicin in oriented phospholipid bilayers determined by N-15 solid-state nuclear magnetic resonance. Biophys. J., 2001, 81,1684-1698.
24. Salnikov, E.S.; Friedrich, H.; Li, X.; Bertani, P.; Reissmann, S.; Hertweck, C.; O'Neil, J. D.; Raap, J.; Bechinger, B. Structure and alignment of the membrane-associated peptaibols ampullosporin A and alamethicin by oriented 15 N and 31 P solid-state NMR spectroscopy. Biophys. J., 2009, 96, 86-100.
25. Huang, H.W. Action of antimicrobial peptides, Two-state model. Biochemistry 2000,39, 8347-8352.
26. Lee, A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta., 2004, 1666, 62-87.
27. Bechinger, B.; Skladnev, D.A.; Ogrel, A.; Li, X.; Swischewa, N.V.; Ovchinnikova, T.V.; O'Neil, J.D.J.; Raap, J. 15 N and 31 P solidstate NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes. Biochemistry, 2001, 40, 9428-9437.
28. Zasloff, M. Antimicrobial peptides in health and disease. N. Engl. J. Med., 2002, 347,1199-1200.
29. Boman, H.G. Antibacterial peptides, basic facts and emerging concepts. J. Intern. Med., 2003, 254,197-215.
30. Garcia-Olmedo, F.; Molina, A.; Alamillo, J. M.; Rodriguez-Palenzuela, P. Plant defense peptides. Biopolymers, 1999, 47, 479-491.
31. Gesell, J.; Zasloff, M.; Opella, S.J. Two-dimensional 1 H NMR experiments show that the 23-residue magainin antibiotic peptide is an a-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J. Biomol. NMR., 1997,127-135.
32. Bechinger, B.; Zasloff, M.; Opella, S. Structure and Dynamics of the Antibiotic Peptide PGLa in Membranes by Multidimensional Solution and Solid-State NMR Spectroscopy. Biophys. J., 1998,74, 981-987.
33. Georgescu, J.; Bechinger, B. NMR structures of the histidine-rich peptide LAH4 in micellar environments, membrane insertion, pHdependent mode of antimicrobial action and DNA transfection. Biophys. J., 2010, 99, 2507-2515
34. Bolintineanu, D.; Hazrati, E.; Davis, H.T.; Lehrer, R.I.; Kaznessis, Y. N. Antimicrobial mechanism of pore-forming protegrin peptides, 100 pores to kill E. coli. Peptides, 2010, 31,1-8.
35. Wade, D.; Andreu, D.; Mitchell, S.A.; Silveira, A.M.; Boman, A.; Boman, H.G.; Merrifield, R. B. Antibacterial peptides designed as analogs or hybrids of cecropins and melittin. Int. J. Pept. Pro. Res., 1992, 40, 429-436.
36. Wade, D.; Boman, A.; Wahlin, B.; Drain, C.M.; Andreu, D.; Boman, H.G.; Merrifield, R.B. All-D amino acid-containing channel-forming antibiotic peptides. Proc. Natl. Acad. Sci. USA., 1990, 87,4761-4765.
37. Hugosson, M.; Andreu, D.; Boman, H.G.; Glaser, E. Antibacterial peptides and mitochondrial presequences affect mitochondrial coupling, respiration and protein import. Euro. J. Biochem., 1994, 223,1027-1033.
38. Westerhoff, H.V.; Juretic, D.; Hendler, R.W.; Zasloff, M. Magainins and the disruption of membrane-linked free-energy transduction. Proc. Natl. Acad. Sci. USA., 1989, 86, 6597-6601.
39. Bechinger, B.; Kim, Y.; Chirlian, L.E.; Gesell, J.; Neumann, J.M.; Montal, M.; Tomich, J.; Zasloff, M.; Opella, S. J. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J. Biomol. NMR., 1991, 1,167-173.
40. Pouny Y, Rapaport D, Mor A, Nicolas P, Shai Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry, 1992, 31,12416-12423.
41. Matsuzaki, K.; Murase, O.; Tokuda, H.; Funakoshi, S.; Fujii, N.; Miyajima, K. Orientational and Aggregational States of Magainin 2 in Phospholipid Bilayers. Biochemistry, 1994, 33, 3342-3349.
42. Ramamoorthy, A.; Thennarasu, S.; Lee, D. K.; Tan, A.; Maloy, L. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J., 2006, 91, 206-216.
43. Strandberg, E.; Kanithasen, N.; Tiltak, D.; Burck, J.; Wadhwani, P.; Zwernemann, O.; Ulrich, A.S. Solid-state NMR analysis comparing the designer-made antibiotic MSI-103 with its parent peptide PGLa in lipid bilayers. Biochemistry, 2008, 47, 2601-2616.
44. Mason, A.J.; Moussaoui, W.; Abdelrhaman, T.; Boukhari, A.; Bertani, P.; Marquette, A.; Shooshtarizaheh, P.; Moulay, G.; Boehm, N.; Guerold, B.; Sawers, R.J.H.; Kichler, A.; Metz-Boutigue, M.H.; Candolfi, E.; Prevost, G.; Bechinger, B. Structural determinants of antimicrobial and antiplasmodial activity and selectivity in histidine rich amphipathic cationic peptides. J. Biol. Chem., 2009, 284, 119-133.
45. Verly, R.M.; Moraes, C.M.; Resende, J.M.; Aisenbrey, C.; Bemquemer, M.P.; Pilo-Veloso, D.; Valente, A.P.; Alemida, F.C.; Bechinger, B. Structure and membrane interactions of the antibiotic peptide dermadistinctin k by solution and oriented 15 N and 31 P solid-state NMR spectroscopy. Biophys. J., 2009, 96, 2194-2202.
46. Resende, J.M.; Mendonca Moraes, C.; Munhoz, V. H. D. O.; Aisenbrey, C.; Verly, R.M.; Bertani, P.; Cesar, A.; Pilo-Veloso, D.; Bechinger, B. Membrane structure and conformational changes during bilayer-association of the antibiotic heterodimeric peptide distinctin by oriented solid-state NMR spectroscopy. Proc. Natl. Acad. Sci. USA., 2009,106, 16639-16644.
47. Bechinger, B.; Resende, J.M.; Aisenbrey, C. The structural and topological analysis of membrane-associated polypeptides by oriented solid-state NMR spectroscopy, Established concepts and novel developments. submitted 2010.
48. Leontiadou, H.; Mark, A.E.; Marrink, S. J. Antimicrobial peptides in action. J. Am. Chem. Soc., 2006,128, 12156-12161.
49. Bechinger, B. Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape. Curr. Opin. Colloid Interface Sci. Surfactants, 2009, 14, 349-355.
50. Salnikov, E.S.; Mason, A.J.; Bechinger, B. Membrane order perturbation in the presence of antimicrobial peptides by 2 H solidstate NMR spectroscopy. Biochimie, 2009, 91,743.
51. Vogt, T.C.B.; Bechinger, B. The interactions of histidinecontaining amphipathic helical peptide antibiotics with lipid bilayers, The effects of charges and pH. J. Biol. Chem., 1999, 274, 29115-29121.
52. Shai, Y. Mechanism of the binding, insertion, and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective lytic peptides. Biochimica. et Biophysica. Acta., 1999, 1462, 55-70.
53. Ludtke, S. J.; He, K.; Heller, W.T.; Harroun, T. A.; Yang, L.; Huang, H. W. Membrane pores induced by magainin. Biochemistry, 1996, 35,13723-13728.
54. Makovitzki, A.; Baram, J.; Shai, Y. Antimicrobial lipopolypeptides composed of palmitoyl Di-and tricationic peptides, in vitro and in vivo activities, self-assembly to nanostructures, and a plausible mode of action. Biochemistry, 2008, 47, 10630-10636.
55. Patch, J. A.; Barron, A. E. Helical peptoid mimics of magainin-2 amide. J. Am. Chem. Soc., 2003,125, 12092-12093.
56. Porter, E. A.; Weisblum, B.; Gellman, S. H. Mimicry of hostdefense peptides by unnatural oligomers, antimicrobial betapeptides. J. Am. Chem. Soc., 2002, 124, 7324-7330.
57. Kuroda, K.; DeGrado, W. F. Amphiphilic polymethacrylate derivatives as antimicrobial agents. J. Am. Chem. Soc., 2005, 127, 4128-4129.
58. Violette, A.; Fournel, S.; Lamour, K.; Chaloin, O.; Frisch, B.; Briand, J. P.; Monteil, H.; Guichard, G. Mimicking helical antibacterial peptides with nonpeptidic folding oligomers. Chem. Biol., 2006, 13, 531-538.
59. Wenk, M.; Seelig, J. Magainin 2 amide interaction with lipid membranes, Calorimetric detection of peptide binding and pore formation. Biochemistry, 1998, 37, 3909-3916.
60. Matsuzaki, K.; Harada, M.; Funakoshi, S.; Fujii, N.; Miyajima, K. Physicochemical Determinants for the Interactions of Magainins 1 and 2 with Acidic Lipid Bilayers. Biochimica. et Biophysica. Acta., 1991, 1063,162-170.
61. Wieprecht, T.; Apostolov, O.; Seelig, J. Binding of the antibacterial peptide magainin 2 amide to small and large unilamellar vesicles. Biophys. Chem. EDAT-2000/08/29 MHDA-2000/08/29 PST-ppublish, 2000, 85,187-198.
62. Bechinger, B. Membrane-lytic peptides. Crit. Rev. Plant Sci., 2004, 23, 271-292.
63. Klocek, G.; Seelig, J. Melittin interaction with sulfated cell surface sugars. Biochemistry, 2008, 47, 2841-2849.
64. Glaser, R.W.; Sachse, C.; Durr, U.H.; Wadhwani, P.; Afonin, S.; Strandberg, E.; Ulrich, A. S. Concentration-dependent realignment of the antimicrobial peptide PGLa in lipid membranes observed by solid-state 19F-NMR. Biophys. J., 2005, 88, 3392-3397.
65. Salnikov, E.; Bechinger, B. Lipid-mediated peptide-peptide interactions in supported bilayers, Structural insights into the synergistic enhancement of the antimicrobial activities of PGLa and magainin2 in preparation 2010.
66. Tremouilhac, P.; Strandberg, E.; Wadhwani, P.; Ulrich, A. S. Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin. J. Biol. Chem., 2006, 281, 32089-32094.
67. Bechinger, B.; Zasloff, M.; Opella, S. J. Structure and Interactions of Magainin Antibiotic Peptides in Lipid Bilayers, A Solid-State NMR Investigation. Biophys. J., 1992, 62, 12-14.
68. Heitz, F.; Morris, M.C.; Divita, G. Twenty years of cell-penetrating peptides, from molecular mechanisms to therapeutics. Br. J. Pharmacol., 2009,157,195-206.
69. Ziegler, A. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv. Drug Deliv. Rev., 2008, 60, 580-597.
70. Tang, M.; Waring, A.J.; Hong, M. Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. J. Am. Chem. Soc., 2007,129, 11438-11446.
71. Henriques, S.T.; Melo, M.N.; Castanho, M.A. Cell-penetrating peptides and antimicrobial peptides, how different are they? Biochem. J., 2006, 399,1-7.
72. Deshayes, S.; Heitz, A.; Morris, M.C.; Charnet, P.; Divita, G.; Heitz, F. Insight into the mechanism of internalization of the cellpenetrating carrier peptide Pep-1 through conformational analysis. Biochemistry, 2004, 43, 1449-1457.
73. Barany-Wallje, E.; Andersson, A.; Graslund, A.; Maler, L. NMR solution structure and position of transportan in neutral phospholipid bicelles. FEBS Lett., 2004, 567, 265-269.
74. Herbig, M. E.; Weller, K.; Krauss, U.; Beck-Sickinger, A. G.; Merkle, H. P.; Zerbe, O. Membrane surface-associated helices promote lipid interactions and cellular uptake of human calcitoninderived cell penetrating peptides. Biophys. J., 2005, 89, 4056-4066.
75. Epand, R. M.; Vogel, H. J. Diversity of antimicrobial peptides and their mechanism of action. Biochimica. et Biophysica. Acta., 1999, 1462, 11-28.
76. Sugawara, M.; Resende, J.M.; Mendonca, M. C.; Marquette, A.; Chich, J. F.; Metz-Boutigue, M. H.; Bechinger, B. Membrane structure and interactions of human Catestatin by multidimensional solution and solid-state NMR spectroscopy. FASEB J., 2010, 24, 1737-1746.
77. Lindberg, M.; Graslund, A. The position of the cell penetrating peptide penetratin in SDS micelles determined by NMR. FEBS Lett., 2001, 497, 39-44.
78. Uezono, T.; Toraya, S.; Obata, M.; Nishimura, K.; Tuzi, S.; Saito, H.; Naito, A. Structure and orientation of dynorphin bound to lipid bilayers by 13C solid-state NMR. J. Mol. Struct., 2005,749, 13-19.
79. Hugonin, L.; Barth, A.; Graslund, A.; Peralvarez-Marin, A. Secondary structure transitions and aggregation induced in dynorphin neuropeptides by the detergent sodium dodecyl sulfate. Biochimica. et Biophysica. Acta., 2008,1778, 2580-2587.
80. Balayssac, S.; Burlina, F.; Convert, O.; Bolbach, G.; Chassaing, G.; Lequin O. Comparison of penetratin and other homeodomainderived cell-penetrating peptides, interaction in a membranemimicking environment and cellular uptake efficiency. Biochemistry, 2006, 45, 1408-1420.
81. Magzoub, M.; Eriksson, L. E.; Graslund, A. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles, effects of surface charge and peptide concentration. Biochimica. et Biophysica. Acta., 2002, 1563, 53-63.
82. Jean-Francois, F.; Castano, S.; Desbat, B.; Odaert, B.; Roux, M.; Metz-Boutigue, M. H.; Dufourc, E. J. Aggregation of cateslytin beta-sheets on negatively charged lipids promotes rigid membrane domains. A new mode of action for antimicrobial peptides? Biochemistry, 2008, 47, 6394-6402.
83. Wi, S.; Kim, C. Pore structure, thinning effect, and lateral diffusive dynamics of oriented lipid membranes interacting with antimicrobial peptide protegrin-1, P-31 and H-2 solid-state NMR study. J. Phys. Chem. B., 2008, 112, 11402-11414.
84. Derossi, D.; Calvet, S.; Trembleau, A.; Brunissen, A.; Chassaing, G.; Prochiantz, A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biologica. Chem., 1996, 271,18188-18193.
85. Bechinger, B.; Ruysschaert, J. M.; Goormaghtigh, E. Membrane Helix Orientation from Linear Dichroism of Infrared Attenuated Total Reflection Spectra. Biophys. J., 1999, 76, 552-563.
86. Aisenbrey, C.; Goormaghtigh, E.; Ruysschaert, J. M.; Bechinger, B. Translocation of amino acyl residues from the membrane interface to the hydrophobic core, Thermodynamic model and experimental analysis using ATR-FTIR spectroscopy. Mol. Memb. Biol., 2006, 23, 363-374.
87. Aisenbrey, C.; Kinder, R.; Goormaghtigh, E.; Ruysschaert, J.M.; Bechinger, B. Interactions involved in the realignment of membrane-associated helices, An investigation using oriented solid-state NMR and ATR-FTIR spectroscopies topologies J. Biol. Chem., 2006, 281, 7708-7716.
88. Kichler, A.; Leborgne, C.; MÑrz, J.; Danos, O.; Bechinger, B. Histidine-rich amphipathic peptide antibiotics promote efficient delivery of DNA into mammalian cells. Proc. Natl. Acad. Sci. USA., 2003, 100, 1564-1568.
89. Marquette, A.; Mason, A. J.; Bechinger, B. Aggregation and membrane permeabilizing properties of designed histidinecontaining cationic linear peptide antibiotics. J. Pept. Sci., 2008, 14, 488-495.
90. Mason, A.J.; Gasnier, C.; Kichler, A.; Prevost, G.; Aunis, D.; Metz-Boutigue, M. H.; Bechinger, B. Enhanced membrane disruption and antibiotic action against pathogenic bacteria by designed histidine-rich peptides at acidic pH. Antimicrob. Agents Chemother., 2006, 50, 3305-3311.
91. Langlet-Bertin, B.; Leborgne, C.; Scherman, D.; Bechinger, B.; Mason, A. J.; Kichler, A. Design and evaluation of histidine-rich amphipathic peptides for siRNA delivery. Pharm. Res., 2010, 27, 1426-1436.
92. Bechinger, B.; Vidovic, V.; Bertani, P.; Kichler, A. A new family of peptide-nucleic acid nanostructures with potent transfection activities. J. Peptide Sci., (in press), 2010.
93. Prongidi-Fix, L.; Sugewara, M.; Bertani, P.; Raya, J.; Leborgne, C.; Kichler, A.; Bechinger, B. Self-promoted uptake of peptide/ DNA transfection complexes. Biochemistry, 2007, 46, 11253-11262.
94. Kichler, A.; Leborgne, C.; Danos, O.; Bechinger, B. Characterization of the gene transfer process mediated by histidinerich peptides. J. Mol. Med., 2007, 85,191-201.
95. Mason, A. J.; Martinez, A.; Glaubitz, C.; Danos, O.; Kichler, A.; Bechinger, B. The antibiotic and DNA-transfecting peptide LAH4 selectively associates with, and disorders, anionic lipids in mixed membranes. FASEB J., 2006, 20, 320-322.
96. Mason, A. J.; Bechinger, B.; Kichler, A. Rational design of vector and antibiotic peptides using solid-state NMR. Mini. Rev. Med. Chem., 2007, 7, 491-497.
97. Mason, A. J.; Leborgne, C.; Moulay, G.; Martinez, A.; Danos, O.; Bechinger, B.; Kichler, A. Optimising histidine rich peptides for efficient DNA delivery in the presence of serum. J. Control Release, 2007, 118, 95-104.
98. Marquette, A.; Lorber, B.; Bechinger, B. Reversible liposome association induced by LAH4, a peptide with potent antimicrobial and nucleic acid transfection activities. Biophys. J., 2010, 98, 2544-2553.
99. Lamaziere, A.; Wolf, C.; Lambert, O.; Chassaing, G.; Trugnan, G.; Yala-Sanmartin, J. The homeodomain derived peptide Penetratin induces curvature of fluid membrane domains. PLoSONE, 2008, 3,e1938.
100. Galanth, C.; Abbassi, F.; Lequin, O.; yala-Sanmartin, J.; Ladram, A.; Nicolas, P.; Amiche, M. Mechanism of antibacterial action of dermaseptin B2, interplay between helix-hinge-helix structure and membrane curvature strain. Biochemistry, 2009, 48, 313-327.
101. Ramamoorthy, A. Beyond NMR spectra of antimicrobial peptides, dynamical images at atomic resolution and functional insights. Solid State Nucl. Magn. Reson., 2009, 35, 201-207.