Metabolic cleavage and translocation efficiency of selected cell penetrating peptides: A comparative study with epithelial cell cultures

AAPS Journal

Volumn 10, Issue 2, 2008, Pages 349-359

  Foerg, Christina ^a   Weller, Kathrin M ^a   Rechsteiner, Helene ^b   Nielsen, Hanne M ^c   Fernández Carneado, Jimena ^d   Brunisholz, René ^b   Giralt, Ernest ^d,e   Merkle, Hans P ^a  

^a ETH ZURICH   (Switzerland)

^b FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cell penetrating peptides; Cellular translocation; Epithelial cell cultures; Metabolic cleavage; Metabolism kinetics

Indexed keywords

AMINO ACID; CELL PENETRATING PEPTIDE;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL STRAIN; COMPARATIVE STUDY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DEGRADATION KINETICS; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE TRANSLOCATION; HELA CELL; HUMAN; HUMAN CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE PERMEABILITY; CULTURE MEDIA, SERUM-FREE; DRUG STABILITY; EPITHELIAL CELLS; FLOW CYTOMETRY; HUMANS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 53849146005     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-008-9029-4     Document Type: Article

References (42)

1. L. A. Kueltzo, and C. R. Middaugh. Potential use of non-classical pathways for the transport of macromolecular drugs. Expert Opin. Investig. Drugs. 9: 2039-2050 (2000).
2. D. Derossi, A. H. Joliot, G. Chassaing, and A. Prochiantz. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269: 10444-10450 (1994).
3. E. Vives, P. Brodin, and B. Lebleu. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272: 16010-16017 (1997).
4. A. Prochiantz. Getting hydrophilic compounds into cells: Lessons from homeopeptides. Curr. Opin. Neurobiol. 6: 629-634 (1996).
5. S. R. Schwarze, A. Ho, A. Vocero-Akbani, and S. F. Dowdy. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science. 285: 1569-1572 (1999).
6. D. Singh, S. K. Bisland, K. Kawamura, and J. Gariepy. Peptide-based intracellular shuttle able to facilitate gene transfer in mammalian cells. Bioconjug. Chem. 10: 745-754 (1999).
7. M. Lewin, N. Carlesso C. H. Tung et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol. 18: 410-414 (2000).
8. A. Astriab-Fisher, D. Sergueev, M. Fisher, B. R. Shaw, and R. L. Juliano. Conjugates of antisense oligonucleotides with the Tat and antennapedia cell-penetrating peptides: Effects on cellular uptake, binding to target sequences, and biologic actions. Pharm. Res. 19: 744-754 (2002).
9. J. A. Fix. Oral controlled release technology for peptides: Status and future prospects. Pharm. Res. 13: 1760-1764 (1996).
10. R. Fischer, K. Kohler, M. Fotin-Mleczek, and R. Brock. A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J. Biol. Chem. 279: 12625-12635 (2004).
11. A. Elmquist, M. Lindgren, T. Bartfai, and U. Langel. VE-cadherin-derived cell-penetrating peptide, pVEC, with carrier functions. Exp. Cell. Res. 269: 237-244 (2001).
12. A. Elmquist, and U. Langel. In vitro uptake and stability study of pVEC and its all-D analog. Biol. Chem. 384: 387-393 (2003).
13. R. Trehin, H. M. Nielsen, H. G. Jahnke, U. Krauss, A. G. Beck-Sickinger, and H. P. Merkle. Metabolic cleavage of cell-penetrating peptides in contact with epithelial models: Human calcitonin (hCT)-derived peptides, Tat(47-57) and penetratin(43-58). Biochem. J. 382: 945-956 (2004).
14. M. E. Lindgren, M. M. Hallbrink, A. M. Elmquist, and U. Langel. Passage of cell-penetrating peptides across a human epithelial cell layer in vitro. Biochem. J. 377: 69-76 (2004).
15. G. Karp. Cell and molecular biology, 2nd edn, John Wiley & Sons, New York, 1999.
16. K. Simons, and S. D. Fuller. Cell surface polarity in epithelia. Annu. Rev. Cell Biol. 1: 243-288 (1985).
17. B. I. Florea, M. L. Cassara, H. E. Junginger, and G. Borchard. Drug transport and metabolism characteristics of the human airway epithelial cell line Calu-3. J. Control Release. 87: 131-138 (2003).
18. L. Crespo, G. Sanclimens B. Montaner et al. Peptide dendrimers based on polyproline helices. J. Am. Chem. Soc. 124: 8876-8883 (2002).
19. J. Fernandez-Carneado, M. J. Kogan, S. Castel, and E. Giralt. Potential peptide carriers: Amphipathic proline-rich peptides derived from the N-terminal domain of gamma-Zein. Angew. Chem. Int. Ed. Engl. 43: 1811-1814 (2004).
20. J. Fernandez-Carneado, M. J. Kogan, S. Pujals, and E. Giralt. Amphipathic peptides and drug delivery. Biopolymers. 76: 196-203 (2004).
21. R. Trehin, U. Krauss, R. Muff, M. Meinecke, A. G. Beck-Sickinger, and H. P. Merkle. Cellular internalization of human calcitonin derived peptides in MDCK monolayers: A comparative study with Tat(47-57) and penetratin(43-58). Pharm. Res. 21: 33-42 (2004).
22. U. Krauss, M. Muller, M. Stahl, and A. G. Beck-Sickinger. In vitro gene delivery by a novel human calcitonin (hCT)-derived carrier peptide. Bioorg. Med. Chem. Lett. 14: 51-54 (2004).
23. C. Foerg, U. Ziegler J. Fernandez-Carneado et al. Decoding the entry of two novel cell-penetrating peptides in HeLa Cells: Lipid Raft-mediated endocytosis and endosomal escape. Biochemistry. 44: 72-81 (2005).
24. P. Vidal, M. C. Morris, L. Chaloin, J. Mery, F. Heitz, and G. Divita. Conformations of a synthetic peptide which facilitates the cellular delivery of nucleic acids. Lett. Pept. Sci. 4: 227-230 (1997).
25. M. C. Morris, P. Vidal, L. Chaloin, F. Heitz, and G. Divita. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res. 25: 2730-2736 (1997).
26. S. Deshayes, T. Plenat, G. Aldrian-Herrada, G. Divita, C. Le Grimellec, and F. Heitz. Primary amphipathic cell-penetrating peptides: Structural requirements and interactions with model membranes. Biochemistry. 43: 7698-7706 (2004).
27. B. Rothen-Rutishauser, S. D. Kramer, A. Braun, M. Gunthert, and H. Wunderli-Allenspach. MDCK cell cultures as an epithelial in vitro model: cytoskeleton and tight junctions as indicators for the definition of age-related stages by confocal microscopy. Pharm. Res. 15: 964-971 (1998).
28. M. C. Morris, V. Robert-Hebmann L. Chaloin et al. A new potent HIV-1 reverse transcriptase inhibitor. A synthetic peptide derived from the interface subunit domains. J. Biol. Chem. 274: 24941-24946 (1999).
29. J. P. Richard, K. Melikov E. Vives et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278: 585-590 (2003).
30. S. Sahlin, J. Hed, and I. Rundquist. Differentiation between attached and ingested immune-complexes by a fluorescence quenching cytofluorometric assay. J. Immunol. Methods. 60: 115-124 (1983).
31. Z. S. Ma, and L. Y. Lim. Uptake of chitosan and associated insulin in Caco-2 cell monolayers: A comparison between chitosan molecules and chitosan nanoparticles. Pharm. Res. 20: 1812-1819 (2003).
32. C. P. Wan, C. S. Park, and B. H. S. Lau. A rapid and simple microfluorometric phagocytosis assay. J. Immunol. Methods. 162: 1-7 (1993).
33. W. C. Tseng, N. B. Purvis, F. R. Haselton, and T. D. Giorgio. Cationic liposomal delivery of plasmid to endothelial cells measured by quantitative flow cytometry. Biotechnol. Bioeng. 50: 548-554 (1996).
34. J. Hed, G. Hallden, S. G. Johansson, and P. Larsson. The use of fluorescence quenching in flow cytofluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation. J. Immunol. Methods. 101: 119-125 (1987).
35. N. P. Innes, and G. R. Ogden. A technique for the study of endocytosis in human oral epithelial cells. Arch. Oral Biol. 44: 519-523 (1999).
36. H. C. Kang, Y. H. Park, and S. J. Go. Growth inhibition of a phytopathogenic fungus, Colletotrichum species by acetic acid. Microbiol. Res. 158: 321-326 (2003).
37. D. S. Youngblood, S. A. Hatlevig, J. N. Hassinger, P. L. Iversen, and H. M. Moulton. Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug. Chem. 18: 50-60 (2007).
38. C. Palm, M. Jayamanne, M. Kjellander, and M. Hallbrink. Peptide degradation is a critical determinant for cell-penetrating peptide uptake. Biochim. Biophys. Acta. 1768: 1769-1776 (2007).
39. B. Q. Shen, W. E. Finkbeiner, J. J. Wine, R. J. Mrsny, and J. H. Widdicombe. Calu-3: A human airway epithelial cell line that shows cAMP-dependent Cl- secretion. Am. J. Physiol. 266: L493-501 (1994).
40. I. I. Forbes. Human airway epithelial cell lines for in vitro drug transport and metabolism studies. Pharm. Sci. Technol. Today. 3: 18-27 (2000).
41. N. R. Mathia, J. Timoszyk, P. I. Stetsko, J. R. Megill, R. L. Smith, and D. A. Wall. Permeability characteristics of calu-3 human bronchial epithelial cells: In vitro - in vivo correlation to predict lung absorption in rats. J. Drug Target. 10: 31-40 (2002).
42. D. E. Chico, R. L. Given, and B. T. Miller. Binding of cationic cell-permeable peptides to plastic and glass. Peptides. 24: 3-9 (2003).