Cellular uptake but low permeation of human calcitonin-derived cell penetrating peptides and Tat(47-57) through well-differentiated epithelial models

Pharmaceutical Research

Volumn 21, Issue 7, 2004, Pages 1248-1256

  Tréhin, Rachel ^a   Krauss, Ulrike ^b   Beck Sickinger, Annette G ^b   Merkle, Hans P ^a   Nielsen, Hanne M ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

cell penetrating peptides; cellular translocation; epi thelial permeability; epithelial metabolism; human calcitonin

Indexed keywords

CARBOXYFLUORESCEIN; MACROGOL 4000; MACROGOL 900; MANNITOL; PENETRATIN[43-58]; PEPTIDE DERIVATIVE; POLYETHYLENE DERIVATIVE; PROTEIN TAT[47-57]; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG PENETRATION; DRUG UPTAKE; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ANALYSIS;

ANIMALS; CALCITONIN; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE PERMEABILITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EPITHELIAL CELLS; FLUORESCEINS; FLUORESCENT DYES; GENE PRODUCTS, TAT; HUMANS; MICROSCOPY, CONFOCAL; PEPTIDE FRAGMENTS;

EID: 3242674408     PISSN: 07248741     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PHAM.0000033013.45204.c3     Document Type: Article

References (34)

1. 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).
2. A. Prochiantz. Getting hydrophilic compounds into cells: lessons from homeopeptides. Curr. Opin. Neurobiol. 6:629-634 (1996).
3. 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).
4. M. A. Bogoyevitch, T. S. Kendrick, D. C. Ng, and R. K. Barr. Taking the cell by stealth or storm? Protein transduction domains (PTDs) as versatile vectors for delivery. DNA Cell Biol. 21:879-894 (2002).
5. C. H. Tung and R. Weissleder. Arginine containing peptides as delivery vectors. Adv. Drug Deliv. Rev. 55:281-294 (2003).
6. 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).
7. S. J. Bolton, D. N. Jones, J. G. Darker, D. S. Eggleston, A. J. Hunter, and F. S. Walsh. Cellular uptake and spread of the cell-permeable peptide penetratin in adult rat brain. Eur. J. Neurosci. 12:2847-2855 (2000).
8. C. Garcia-Echeverria, L. Jiang, T. M. Ramsey, S. K. Sharma, and Y. P. Chen. A new Antennapedia-derived vector for intracellular delivery of exogenous compounds. Bioorg. Med. Chem. Lett. 11:1363-1366 (2001).
9. H. Nagahara, A. M. Vocero-Akbani, E. L. Snyder, A. Ho, D. G. Latham, N. A. Lissy, M. Becker-Hapak, S. A. Ezhevsky, and S. F. Dowdy. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kipl induces cell migration. Nat. Med. 4:1449-1452 (1998).
10. 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).
11. M. Pooga, U. Soomets, M. Hallbrink, A. Valkna, K. Saar, K. Rezaei, U. Kahl, J. X. Hao, X. J. Xu, Z. Wiesenfeld-Hallin, T. Hokfelt, T. Bartfai, and U. Langel, Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat. Biotechnol. 16:857-861 (1998).
12. U. Kopperhus, S. K. Awasthi, V. Zachar, H. U. Holst, P. Ebbesen, and P. E. Nielsen. Cell-dependent differential cellular uptake of PNA. peptides, and PNA- peptide conjugates. Antisense Nucleic Acid Drug Dev. 12:51-63 (2002).
13. V. P. Torchilin, R. Rammohan, V. Weissig, and T. S. Levchenko. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc. Natl. Acad. Sci. U.S.A. 98:8786-8791 (2001).
14. L. Josephson, C. H. Tung, A. Moore, and R. Weissleder. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug. Chem. 10:186-191 (1999).
15. R. Trehin, U. Krauss, R. Muff, M. Meinecke, A. 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).
16. S. Lang, B. Rothen-Rutishauser, J. C. Perriard, C. Schmidt, and H. P. Merkle. Permeation and pathways of human calcitonin (hCT) across excised bovine nasal mucosa. Peptides 19:599-607 (1998).
17. M. C. Schmidt, B. Rothen-Rutishauser, B. Rist, A. Beck-Sickinger, H. Wunderli-Allenspach, W. Rubas, W. Sadee, and H. P. Merkle. Translocation of human calcitonin in respiratory nasal epithelium is associated with self-assembly in lipid membrane. Biochemistry 37:16582-16590 (1998).
18. Z. Machova, C. Muhle, U. Krauss, R. Trehin ,. Koch, H. P. Merkle, and A. G. Beck-Sickinger. Cellular internalization of enhanced green fluorescent protein ligated to a human calcitonin-based carrier peptide. Chembiochem 3:672-677 (2002).
19. S. Violini, V. Sharma, J. L. Prior, M. Dyszlewski, and D. Piwnica-Worms. Evidence for a plasma membrane-mediated permeability barrier to tat basic domain in well-differentiated epithelial cells: lack of correlation with heparan sulfate. Biochemistry 41:12652-12661 (2002).
20. S. D. Krämer and H. Wunderli-Allenspach. No entry for TAT(44-57) into liposomes and intact MDCK cells: novel approach to study membrane permeation of cell-penetrating peptides. Biochim. Biophys. Acta 1609:161-169 (2003).
21. 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).
22. M. J. Cho, D. P. Thompson, C. T. Cramer, T. J. Vidmar, and J. F. Scieszka. The Madin Darby canine kidney (MDCK) epithelial cell monolayer as a model cellular transport barrier. Pharm. Res. 6:71-77 (1989).
23. 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. Cell Physiol. 266:493-501 (1994).
24. N. R. Mathias, 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).
25. 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. Rel. 7:131-138 (2003).
26. H. T. Rupniak, C. Rowlatt, E. B. Lane, J. G. Steele, L. K. Trejdosiewicz, B. Laskiewicz, S. Povey, and B. T. Hill. Characteristics of four new human cell lines derived from squamous cell carcinomas of the head and neck. J. Natl. Cancer Inst. 75:621-635 (1985).
27. J. Jacobsen, B. V. Deurs, M. Pedersen, and M. R. Rassing. TR146 cells grown on filters as a model for human buccal epithelium: I. Morphology, growth, barrier properties, and permeability. Int. J. Pharm. 125:165-184 (1995).
28. H. M. Nielsen, J. C. Verhoef, M. Ponec, and M. R. Rassing. TR146 cells grown on filters as a model of human buccal epithelium: permeability of fluorescein isothiocyanate-labelled dextrans in the presence of sodium glycocholate. J. Control. Rel. 60:223-233 (1999).
29. B. Rist, M. Entzeroth, and A. G. Beck-Sickinger. From micromolar to nanomolar affinity: A systematic approach to identify the binding site of CGRP at the human calcitonin gene-related peptide 1 receptor. J. Med. Chem. 41:117-123 (1998).
30. 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).
31. H. M. Nielsen and M. R. Rassing. TR146 cells grown on filters as a model of human buccal epithelium: III. Permeability enhancement by different pH values, different osmolality values, and bile salts. Int. J. Pharm. 185:215-225 (1999).
32. S. Lang, P. Langguth, R. Oschmann, B. Traving, and H. P. Merkle. Transport and metabolic pathway of thymocartin (TP4) in excised bovine nasal mucosa. J. Pharm. Pharmacol. 48:1190-1196 (1996).
33. T. Suzuki, S. Futaki, M. Niwa, S. Tanaka, K. Ueda, and Y. Sugiura. Possible existence of common internalization mechanisms among arginine- rich peptides. J. Biol. Chem. 277:2437-2443 (2002).
34. H. Jia, M. Lohr, S. Jezequel, D. Davis, S. Shaikh, D. Selwood, and I. Zachary. Cysteine-rich and basic domain HIV-1 Tat peptides inhibit angiogenesis and induce endothelial cell apoptosis. Biochem. Biophys. Res. Commun. 283:469-479 (2001).