Insight into the Mechanism of Internalization of the Cell-Penetrating Carrier Peptide Pep-1 through Conformational Analysis

Biochemistry

Volumn 43, Issue 6, 2004, Pages 1449-1457

  Deshayes, Sébastien ^a   Heitz, Annie ^b   Morris, May C ^a   Charnet, Pierre ^a   Divita, Gilles ^a   Heitz, Frédéric ^a  

^a Centre National de la Recherche Scientifique   (France)

^b CENTRE DE BIOCHIMIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; CELLS; COMPLEXATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPIDS; POLYPEPTIDES; PROTEINS;

MAMMALIAN CELLS; PEPTIDE CARRIERS;

BIOCHEMISTRY;

CARRIER PROTEIN; PEPTIDE; PROTEIN PEP 1; UNCLASSIFIED DRUG;

ADSORPTION; ALPHA HELIX; ARTICLE; CELL CULTURE; CELL MEMBRANE; CIRCULAR DICHROISM; GENE DELIVERY SYSTEM; INFRARED SPECTROSCOPY; INTERNALIZATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION;

AIR; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL MEMBRANE PERMEABILITY; CIRCULAR DICHROISM; DETERGENTS; FEMALE; LIPID BILAYERS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OOCYTES; PEPTIDES; PHOSPHOLIPIDS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TRANSPORT; SPECTROMETRY, FLUORESCENCE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PROPERTIES; WATER; XENOPUS LAEVIS;

ANIMALIA; MAMMALIA;

EID: 1042288299     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035682s     Document Type: Article

References (44)

1. Ford, K. G., Souberbielle, B. E., Darling, D., and Farzaneh, F. (2001) Protein transduction: an alternative to genetic intervention? Gene Ther. 8, 1-4.
2. Wadia, J. S., and Dowdy, S. F. (2002) Protein transduction technology, Curr. Opin. Biotechnol. 13, 52-56.
3. Morris, M. C., Chaloin, L., Heitz, F., and Divita, G. (2000) Translocating peptides and proteins and their use for gene delivery, Curr. Opin. Biotechnol. 11, 461-466.
4. Gariepy, J., and Kawamura, K. (2001) Vectorial delivery of macromolecules into cells using peptide-based vehicles, Trends Biotechnol. 19, 21-28.
5. Lindgren, M., Hällbrink, M., and Langel, Ü. (2002) Quantification of cell-penetrating peptides and their cargoes, in Cell-Penetrating Peptides: Processes and Applications (Langel, U., Ed.) pp 263-275, CRC Press, Boca Raton, FL.
6. Schwarze, S. R., and Dowdy, S. F. (2000) In vivo protein transduction: intracellular delivery of biologically active proteins, compounds and DNA, Trends Pharmacol. Sci. 21, 45-48.
7. (2002) in Cell-Penetrating Peptides: Processes and Applications. (Langel, U., Ed.) CRC Press, Boca Raton, FL.
8. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse, Science 285, 1569-1572.
9. Gratton, J. P., Yu, J., Griffith, J. W., Babbitt, R. W., Scotland, R. S., Hickey, R., Giordano, F. J., and Sessa, W. C. (2003) Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo, Nat. Med. 9, 357-362.
10. Derossi, D., Joliot, A. H., Chassaing, G., and Prochiantz, A. (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes, J. Biol. Chem. 269, 10444-10450.
11. Elliott, G., and O'Hare, P. (1997) Intercellular trafficking and protein delivery by a herpes virus structural protein, Cell 88, 223-233.
12. Pooga, M., Kut, C., Kihlmark, M., Hallbrink, M., Fernaeus, S., Raid, R., Land, T., Hallberg, E., Bartfai, T., and Langel, Ü. (2001) Cellular translocation of proteins by transportan, FASEB J. 15, 1451-1453.
13. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery, J. Biol. Chem. 276, 5836-5840.
14. Morris, M. C., Depollier, J., Mery, J., Heitz, F., and Divita, G. (2001) A peptide carrier for the delivery of biologically active proteins into mammalian cells, Nat. Biotechnol. 19, 1173-1176.
15. Gallo, R. C., Burny, A., and Zagury, D. (2002) Targeting Tat and IFN(alpha) as a therapeutic AIDS vaccine, DNA Cell. Biol. 21, 611-618.
16. Kowolik, C. M., Yam, P., Yu, Y., and Yee, J.-K. (2003) HIV vector production by Rev protein transduction, Mol. Ther. 8, 324-331.
17. Wu, Y., Wood, M. D., Yi, T., and Katagiri, F. (2002) Direct delivery of bacterial a virulence proteins into resistant Arabidopsis protoplasts leads to hypersensitive cell death, Plant J. 33, 131-137.
18. Pratt, R. L., and Kinch, M. S. (2002) Activation of the EphA2 tyrosine kinase stimulates the MAP/ERK kinase signaling cascade, Oncogene 21, 7690-7699.
19. Aoshiba, K., Yokohori, N., and Nagai, A. (2003) Alveolar wall apoptosis causes lung destruction and emphysematous changes. Am. J. Respir. Cell. Mol. Biol. 28, 555-562.
20. Derossi, D., Chassaing, G., and Prochiantz, A. (1998) Trojan peptides: the penetratin system for intracellular delivery, Trends Cell. Biol. 8, 84-87.
21. Magzoub, M., Kilk, K., Eriksson, L. E., Langel, Ü., and Gräslund; A. (2001) Interaction and structure induction of cell-penetrating peptides in the presence of phospholipid vesicles, Biochim. Biophys. Acta 1512, 77-89.
22. Magzoub, M., Eriksson, L. E., and Gräslund, A. (2003) Comparison of the interaction, positioning, structure induction and membrane perturbation of cell-penetrating peptides and nontranslocating variants with phospholipid vesicles, Biophys. Chem. 103, 271-288.
23. Ziegler, A., Blatter, X. L., Seelig, A., and Seelig, J. (2003) Protein transduction domains of HIV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic analysis, Biochemistry 42, 9185-9194.
24. Ho, A., Schwarze, S. R., Mermelstein, S. J., Waksman, G., and Dowdy, S. F. (2001) Synthetic protein transduction domains: enhanced transduction potential in vitro and in vivo, Cancer Res. 61, 474-477.
25. Morris, M. C., Vidal, P., Chaloin, L., Heitz, F., and (1997) Divita, G. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells, Nucleic Acids Res. 25, 2730-2736.
26. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons Inc., New York.
27. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR. 2, 661-665.
28. Van Mau, N., Vie, V., Chaloin, L., Lesniewska, E., Heitz, F., and Le Grimellec, C. (1999) Lipid-induced organization of a primary amphipathic peptide: a coupled AFM-monolayer study, J. Membr. Biol. 167, 241-249.
29. Vie, V., Van Mau, N., Chaloin, L., Lesniewska, E., Le Grimellec, C., and Heitz, F. (2000) Detection of peptide-lipid interactions in mixed monolayers, using isotherms, atomic force microscopy, and Fourier transform infrared analyses, Biophys. J. 78, 846-856.
30. Morris, M. C., Chaloin, L., Méry, J., Heitz, F., and Divita, G. (1999) A novel potent strategy for gene delivery using a single peptide vector as a carrier, Nucleic Acids Res. 27, 3510-3517.
31. Chaloin, L., De, E., Charnet, P., Molle, G., and Heitz, F. (1998) Ionic Channels Formed by Primary Amphipathic Peptides, Biochim. Biophys. Acta 1375, 52-60.
32. (1996) in Circular Dichroism and the Conformational Analysis of Biomolecules, (Fasman, G. D., Ed.) Plenum Press, New York.
33. Briggs, M. S., Cornell, D. G., Dluhy, R. A., and Gierasch, L. M. (1986) Conformations of signal peptides induced by lipids suggest initial steps in protein export, Science 233, 206-208.
34. Tamm, L. K., and Tatulian, S. A. (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers, Q. Rev. Biophys. 33, 365-429.
35. Fringeli, U. P., and Fringeli, M. (1979) Pore formation in lipid membranes by alamethicin, Proc. Natl. Acad. Sci. U.S.A. 76, 3852-3856.
36. Kennedy, D. F., Crisma, M., Toniolo, C., and Chapman, D. (1991) Studies of peptides forming 3(10)- and alpha-helices and beta-bend ribbon structures in organic solution and in model biomembranes by Fourier transform infrared spectroscopy, Biochemistry 30, 6541-6548.
37. Vidal, P., Chaloin, L., Heitz, A., Van Mau, N., Mery, J., Divita, G., and Heitz, F. (1998) Conformational analysis of primary amphipathic carrier peptides and origin of the various cellular localizations, J. Membrane Biol. 162, 259-264.
38. Chaloin, L., Vidal, P., Heitz, A., Van Mau, N., Mery, J., Divita, G., and Heitz, F. (1997) Conformations of primary amphipathic carrier peptides in membrane mimicking environments, Biochemistry 36, 11179-11187.
39. Demel, R. A., Geurts van Kessel, W. S., Zwaal, R. F., Roelofsen, B., and van Deenen, L. L. (1975) Relation between various phospholipase actions on human red cell membranes and the interfacial phospholipid pressure in monolayers, Biochim. Biophys. Acta 406, 97-107.
40. (1983) in Principles of Fluorescence Spectroscopy. (Lakowicz, J. R., Ed.) Plenum Press, New York.
41. Richard, J. P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M. J., Chernomordik, L. V., and Lebleu, B. (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake, J. Biol Chem. 278, 585-590.
42. Bellet-Amalric, E., Blaudez, D., Desbat, B., Graner, F., Gauthier, F., and Renault, A. (2000) Interaction of the third helix of Antennapedia homeodomain and a phospholipid monolayer, studied by ellipsometry and PM-IRRAS at the air-water interface, Biochim. Biophys. Acta 1467, 131-143.
43. Dom, G., Shaw-Jackson, C., Matis, C., Bouffioux, O., Picard, J. J., Prochiantz, A., Mingeot-Leclercq, M. P., Brasseur, R., and Rezsohazy, R. (2003) Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation, Nucleic Acids Res. 31, 556-561.
44. Wang, J., Smerdon, S. J., Jager, J., Kohlstaedt, L. A., Rice, P. A., Friedman, J. M., and Steitz, T. A. (1994) Structural basis of asymmetry in the human immunodeficiency virus typel reverse transcriptase heterodimer, Proc. Natl. Acad. Sci. U.S.A. 91, 7242-7246.