Interactions of primary amphiphatic cell penetrating peptides with model membranes: Consequences on the mechanisms of intracellular delivery of therapeutics

Current Pharmaceutical Design

Volumn 11, Issue 28, 2005, Pages 3629-3638

  Deshayes, Sébastian ^a   Morris, May C ^a   Divita, Gilles ^a   Heitz, Frédéric ^a  

^a Centre National de la Recherche Scientifique   (France)

Author keywords

Lipid monolayers; Peptide conformation; Peptide lipid interactions; Peptide mediated delivery; Spectoscopy

Indexed keywords

BACTERIAL TOXIN; CALCITONIN; CARRIER PROTEIN; CELL PENETRATING PEPTIDE; DODECYL SULFATE SODIUM; PENETRATIN; PHOSPHOLIPID; TIOPRONIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; PEPTIDE;

ALGORITHM; ATOMIC FORCE MICROSCOPY; CELL MEMBRANE TRANSPORT; CELL PERMEABILIZATION; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DRUG DESIGN; GEL MOBILITY SHIFT ASSAY; GENE TRANSLOCATION; INTERNALIZATION; INTRACELLULAR TRANSPORT; ION PERMEABILITY; LANGMUIR BLODGETT FILM; LIPID BILAYER; LIPID MONOLAYER; MASS SPECTROMETRY; MEMBRANE MODEL; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; NUCLEIC ACID TRANSPORT; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; STOICHIOMETRY; TRANSPORT KINETICS; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; DRUG DELIVERY SYSTEM; HUMAN; METABOLISM; PROTEIN CONFORMATION; SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; DRUG DELIVERY SYSTEMS; HUMANS; PEPTIDES; PHOSPHOLIPIDS; PROTEIN CONFORMATION;

EID: 27744443447     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161205774580741     Document Type: Review

References (75)

1. Lindgren M, Hällbrink M, Prochiantz A, Langel Ü. Cell-penetrating peptides. Trends Pliammol Sci 2000; 21: 99-103.
2. Wadia, JS, Dowdy SF. Protein transduction technology. Curr Opin Biotechnol 2002; 13: 52-6.
3. Dom G, Shaw-Jackson C, Matis C, Bouffioux O, Picard JJ, Prochiantz A, et al. Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation. Nucleic Acids Res 2003; 31: 556-61.
4. Cartier R, Reszka R. Utilization of synthetic peptides containing nuclear localization signals for nonviral gone transfer systems. Gene Ther 2002; 9: 157-67.
5. Truatrt R, Cullen BR. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol Cell Biol 1999; 19:1210-7.
6. Rudolph C, Plank C, Lausier J, Schillinger U, Muller RH, Rosenecker J. Oligomers of the arginine-rich motif of the HIV- 1 TAT protein are capable of transferring ptasmid DNA into cells. J Biol Chem 2003; 278: 11411-8.
7. Oehlke J, Birth P, Klauschenz E, Wiesner B, Beyermann M, Oksche A, et al. Cellular uptake of antisense oligonucleotides after complexing or conjugation with cell-penetrating model peptides. Eur J Biochem 2002; 269: 4025-32.
8. Rittner K, Benavente, A, Bompard-Sorlet A, Heitz F, Divita G, Brasseur It, et al. New basic membrime-destabilizing peptides for plasmid-based gene delivery in vitro and in vivo. Mol Ther 2002; 5: 104-14.
9. Sheldon K, Liu D, Ferguson J, Gariépy J. Lotigomers: design of de novo peptide-based intracellular vehicles. Proc, Natl Acad Sci USA 1995; 92: 2056-60.
10. Elliott G, O'Hare P. Intercellular trafficking and protein delivery by a berpesvirus structural protein. Cell 1997; 88: 223-33.
11. Pooga M, Kut C, Kililmark M, Hallbrink M, Famacus S, Raid R, et al. Cellular trauslocation of proteins by transportan. FASEB J 2001; 15: 1451-3.
12. Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, Ueda K, et al. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 2001; 276:5836-40.
13. Fernandez-Carneado, J, Kogan W, Pujals S, Giralt E. Amphipathic peptides and drug delivery. Biopolymers 2004; 76: 196-203.
14. Kogan MJ, Dalcol I, Gorostiza P, Lopez-Iglesias C, Pons R, Pons M, et al. Suptumolecular properties of the proline-rich garraria-Zein N-terminal domain. Biophys J 2002; 83: 1194-204.
15. Trehin R, Krauss U, Muff R, Meinecke M, Beck-Sickinger AG, Merkle HP. Cellular internalization of human calcitonin derived peptides in MDCK monolayers: a comparative Study with Tat(47-57) and penetratin(43-58). Pharm Res 2004; 21: 33-42.
16. Langer M, Beck-Sickinger AG. Peptides as carrier for tumor diagnosis and treatment. Curr Med Chem Anti-Canc Agents 2001; 1: 71-93.
17. Schmidt MC, Rothen-Rutishauser B, Rist B, Beck-Sickinger A, Wunderli-Allenspach H, Rubas W, et al. Translocation of human calcitonin in respiratory nasal epithelium is associated with, self-assembly in lipid membrane. Biochemistry 1999; 37:16582-90.
18. Slepushkin VA, Andreev SM, Sidorova MV, Melikyan GB, Grigoriev VB, Chumakov VM, et al Investigation of human immunodeficiency virus fusion peptides. Analysis of interrelations between their structure and function. AIDS Res Hum Retroviruses 1992; 8: 9-18.
19. Goldfarb DS, Gariépy J, Schoolnik G. Komberg RD. Synthetic peptides as nuclear localization signals. Nature 1986; 322: 641-4.
20. Morris MC, Vidal P, Chaloin L, Heitz F, Divita G. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res 1997; 25: 2730-6.
21. Morris MC, Chaloin L, Mery J, Heitz F, Divita G. A novel potent strategy for gene delivery using a single peptide vector as a carrier. Nucleic Acids Res 1999; 27: 3510-7.
22. Morris MC, Chaloin L, Heitz F, Divita G. Translocating peptides and proteins and their use for gene delivery. Curr Opin Biotechnol 2000; 11: 461-6.
23. Simeoni F, Morris MC, Heitz F, Divita G. Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res 2003; 31: 2717-24.
24. Morris KV, Chan SW, Jacobsen SE, Looney DJ. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 2004; 305: 1289-92.
25. Morris MC, Depollier J, Mery J, Heitz F, Divita G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 2001 19: 1173-6.
26. Morris MC, Chaloin L, Choob M, Archdeacon J, Heitz F, Divita G. Combination of a new generation of PNAs with a peptide-based carrier enables efficient targeting of cell cycle progression. Gene Ther 2004; 11: 757-64.
27. Basak A, Dong F, Basak S. In: Chorev M, Sawyer TK Eds, Proc 18th American Peptide Symposium. San Diego, American Peptide Society. 2004; 343-5.
28. Vidal P, Chaloin L, Mery J, Lamb N, Lautredou N, Bennes R, et al. Solid-phase synthesis and cellular localization of a C- and/or N-terminal labelled peptide, J Pept Sci 1996; 2: 125-33.
29. Munoz V, Serrano L. Development of the multiple sequence approximation within the AGADIR model of alpha-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 1997; 41: 495-509.
30. Greenfield N, Fasman GD. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 1969; 8: 4108-16.
31. Deshayes S, Plenat T, Aldrian-Herrada G, Divita G, Le Grimellec C, Heitz F. Primary amphipathip cell-penetrating peptides: structural requirements and interactions with model membranes. Biochemistry 2004; 43: 7698-706.
32. Deshayes S, Heitz A, Morris MC, Charnet P, Divita G, Heitz F. Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis. Biochemistry 2004; 43: 1449-57.
33. Lindberg M, Jarvet J, Langel Ü, Graslund A. Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 2001; 40: 3141-9.
34. Magzoub M, Kilk K, Eriksson LE, Langel Ü, Graslund A. Interaction and structure induction of cell-penetrating peptides in the presence of phospholipid vesicles. Biochim Biophys Acta 2001; 1512: 77-89.
35. Vidal P, Chaloin L, Heitz A, Van Mau N, Mery J, Divita G, et al. F. Interactions of primary amphipathic vector peptides with membranes. Conformational consequences and influence on cellular localization. J Membr Biol 1998; 162: 259-64.
36. Brockman H. Lipid monolayers: why use half a membrane to characterize protein-membrane interactions? Curr Opin Struct Biol 1999; 9: 438-43.
37. Demel RA, Geurts van Kessel WS, Zwaal RF, Roelofsen B, van Deenen LL. Relation between various phospholipase actions on human red cell membranes and the interfacial phospholipid pressure in monolayers. Biochim Biophys Acta 1975; 406: 97-107.
38. Maget-Dana R. The monolayer technique: a potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes. Biochim Biophys Acta 1999; 1462: 109-40.
39. Ruano ML, Nag K, Worthman LA, Casals C, Pérez-Gil J, Keough KMW. Differential partitioning of pulmonary surfactant protein SP-A into regions of monolayers of dipaimitoylphosphatidylcholine and dipaimitoylphosphatidyleholine / dipahnitoylphosphatidylglycerol. Biophys J 1998; 74: 1101-9.
40. Crisp DJ. In: Crisp DJ Ed, Surface Chemistry. London, Butterworths. 1949; 17-35.
41. Gaines GL. In: Prigogine I Ed, Insoluble Monolayers at Liquid-Gas Interfaces. New York, Wiley Interscience. 1966; 281-300.
42. Edidin M. Lipid microdomains in cell surface membranes. Curr Opin Struct Biol 1997; 7: 528-32.
43. Zasadzinski JA, Viswanathan R, Madsen L, Garnaes J, Schwartz DK. Langmuir-Blodgett films. Science 1994; 263: 1726-33.
44. Mou JD, Czajkowsky M, Shao Z. Gramicidin A aggregation in supported gel state phosphatidyleholine bilayers. Biochemistry 1996; 35: 3222-6.
45. ten Grotenhuis E, Demel RA, Ponec M, Boer DR, van Miltenburg JC, Bouwstra JA. Phase behavior of stratum corneum lipids in mixed Langmuir-Blodgett monolayers. Biophys J 1996; 71: 1389-99.
46. Vié V, Van Mau N, Lesniewska E, Goudonnet JP, Heitz F, Le Grimellec C. Distribution of ganglioside GM1 between two-component, two-phase phosphatidylcholine monolayers. Langmuir 1998; 14: 4574-83.
47. Gliss C, Clausen-Schaumann H, Gunther R, Odenbach S, Randl O, Bayerl TM. Direct detection of domains in phospholipid bilayers by grazing incidence diffraction of neutrons: and atomic force microscopy. Biophys J 1998; 74: 2443-50.
48. Hollars CW, Dunn RC. Submicron structure in L-alpha-dipalmitoylphosphatidylcholine monolayers and bilayers probed with confocal, atomic force, and near-field microscopy. Biophys J 1998; 75: 342-53.
49. Hui SW, Viswanathan R, Zasadzinski JA, Israelachvili JN. The structure and stability of phospholipid bilayers by atomic force microscopy. Biophys J 1995; 68: 171-8.
50. Plénat T, Deshayes S, Boichot S, Milhiet PE, Cole RB, Heitz F, et al. Interaction of primary amphipathic cell-penetrating peptides with phospholipid-supported monolayers. Langmuir 2004; 20: 9255-61.
51. Li Y, Heitz F, Le Grimellec C, Cole RB. Hydrophobic component in noncovalent binding of fusion peptides to lipids as observed by electrospray mass spectrometry. Rapid Commun Mass Spectrom 2004; 18: 135-7.
52. Li Y, Heitz F, Le Grimellec C, Cole RB. Lipid-peptide non-covalent interactions observed by nano-electrospray FT-ICR. Anal Chem 2005; 77: 1556-65.
53. Lakowicz JR. In: Lakowicz JR Ed, Principles of Fluorescence Spectroscopy. New York, Plenum Press. 1983.
54. Deshayes S, Gerbal-Chaloin S, Morris MC, Aldrian-Herrada G, Charnet P, Divita G, et al. On the mechanism of non-endosomial peptide-mediated cellular delivery of nucleic acids. Biochim Biophys Acta 2004; 1667: 141-7.
55. Marthinet E, Divita G, Bernaud J, Rigal D, Baggetto L. Modulation of the typical multidrug resistance phenotype by targeting the MED-1 region of human MDR1 promoter. Gene Ther 2000; 7: 1224-33.
56. Deshayes S, Van Mau N, Morris MC, Divita G, Heitz F. In: Chorev M, Sawyer TK Eds, Proc 18th American Peptide Symposium. San Diego, American Peptide Society. 2004; 802-5.
57. Chaloin L, Dé E, Charnet P, Molle G, Heitz F. Ionic channels formed by a primary amphipathic peptide containing a signal peptide and a nuclear localization sequence. Biochim Biophys Acta 1998; 1375: 52-60.
58. Chaloin L, Vidal, P, Heitz A, Van Mau N, Mery J, Divita G, et al. Conformations of primary amphipathic carrier peptides in membrane mimicking environments. Biochemistry 1997; 36: 11179-87.
59. Henriques ST, Castanho MA. Consequences of nonlytic membrane perturbation to the translocation of the cell penetrating peptide pep-1 in lipidic vesicles. Biochemistry 2004; 43: 9716-24.
60. Joliot AH, Triller A, Volovich M, Pernelle C, Prochiantz A. alpha-2,8-Polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide. New Biol 1991; 3: 1121-34.
61. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994; 269: 10444-50.
62. Prochiantz A. Getting hydrophilic compounds into cells: lessons from homeopeptides. Curr Opin Neurobiol 1996; 6: 629-34.
63. Pooga M, Soomets U, Hällbrink M, Valkna A, Saar K, Rezai K, et al. Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat Biotechnol 1998; 16: 857-61.
64. Derossi D, Chassaing G, Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol 1998; 8: 84-7.
65. Dupont E, Joliot A, Prochiantz A. In: Langel Ü Ed, Cell-Penetrating Peptides: Processes and Applications. Boca Raton, CRC Press. 2002; 23-31.
66. Binder H, Lindblom G. Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes. Biophys J 2003; 85: 982-95.
67. Wagner K, Van Mau N, Boichot S, Kajava AV, Krauss U, Le Grimellec C, et al. Interactions of the human calcitonin-fragment 9-32 with phospholipids: a monolayer study. Biophys J 2004; 87: 386-95.
68. Wagner K, Beck-Sickinger A. Huster D. Structural investigations of a human calcitonin-derived carrier peptide in a membrane environment by solid-state NMR. Biochemistry 2004; 43: 12459-68.
69. Boichot S, Krauss U, Plenat T, Rennert R, Milhiet PE, Beck-Sickinger A, et al. Calcitonin-derived carrier peptide plays a major role in the membrane localization of a peptide-cargo complex. FEBS Lett 2004; 569: 346-50.
70. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10: 310-5.
71. Thorén PEG, Persson D, Esbjöner EK, Goksör M, Lincoln P, Nordén B. Membrane binding and translocation of cellpenetrating peptides. Biochemistry 2004; 43: 3471-89.
72. Fischer R, Kohler K, Fotin-Mleczek M., Brock R. A stepwise dissection of the intracellular fate of cationic, cell-penetrating peptides. J Biol Chem 2004;279: 12625-35.
73. Irani BG, Holder JR, Todorovic A, Wilczynski AM, Joseph CG, Wilson KR, et al. Progress in the development of melanocortin receptor selective ligands. Curr Pharm Design 2004; 10(28): 3443-79.
74. Krishnadas A, Onyuksel H, Rubinstein I. Interactions of VIP, secretin and PACAP(1-38) with phospholipids: a biological paradox revisited. Curr Pharm Design 2003; 9(12): 1005-12.
75. Stefanidakis M, Koivunen E. Peptide-mediated delivery of therapeutic and imaging agents into mammalian cells. Curr Pharm Design 2004; 10(24): 3033-44.