A comprehensive model for the cellular uptake of cationic cell-penetrating peptides

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Volumn 8, Issue 7, 2007, Pages 848-866

  Duchardt, Falk ^a   Fotin Mleczek, Mariola ^a   Schwarz, Heinz ^b   Fischer, Rainer ^a   Brock, Roland ^a,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antennapedia homeodomain; Cell penetrating peptide; Endocytosis; Oligo arginine; TAT

Indexed keywords

ANTENNAPEDIA PROTEIN; ARGININE; CATION; CELL PENETRATING PEPTIDE; CHLORPROMAZINE; CLATHRIN; DYNAMIN; HEPARIN LYASE; HOMEODOMAIN PROTEIN; ROTTLERIN; TRANSACTIVATOR PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; HUMAN; HUMAN CELL; LIPID RAFT; MOLECULAR MODEL; MOUSE; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

APOPTOSIS; ARGININE; CATIONS; CELL MEMBRANE; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; GENE PRODUCTS, TAT; HELA CELLS; HIV-1; HUMANS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; PEPTIDES; PROTEIN TRANSPORT;

EID: 34250835903     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00572.x     Document Type: Article

References (56)

1. Joliot A, Pernelle C, Deagostini-Bazin H, Prochiantz A. Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci USA 1991; 88: 1864-1868.
2. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55: 1189-1193.
3. Malecki J, Wesche J, Skjerpen CS, Wiedlocha A, Olsnes S. Translocation of FGF-1 and FGF-2 across vesicular membranes occurs during G1-phase by a common mechanism. Mol Biol Cell 2004; 15: 801-814.
4. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994; 269: 10444-10450.
5. Vives E, Brodin P, Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 1997; 272: 16010-16017.
6. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB. Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 2000; 56: 318-325.
7. Dietz GPH, Bähr M. Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 2004; 27: 85-131.
8. Snyder EL, Dowdy SF. Cell penetrating peptides in drug delivery. Pharm Res 2004; 21: 389-393.
9. Prochiantz A. Messenger proteins: Homeoproteins, TAT and others. Curr Opin Cell Biol 2000; 12: 400-406.
10. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J. Studies on the internalization mechanism of cationic cell-penetrating peptides. J Biol Chem 2003; 278: 31192-31201.
11. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. Cell-penetrating peptides: A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003; 278: 585-590.
12. Vendeville A, Rayne F, Bonhoure A, Bettache N, Montcourrier P, Beaumelle B. HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses. Mol Biol Cell 2004; 15: 2347-2360.
13. Console S, Marty C, Garcia-Echeverria C, Schwendener R, Ballmer-Hofer K. Antennapedia and HIV TAT "protein transduction domains"promote endocytosis of high Mr cargo upon binding to cell surface glycosaminoglycans. J Biol Chem 2003; 278: 35109-35114.
14. Ziegler A, Seelig J. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: Binding mechanism and thermodynamic parameters. Biophys J 2004; 86: 254-263.
15. 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: 310-315.
16. Ferrari A, Pellegrini V, Arcangeli C, Fittipaldi A, Giacca M, Beltram F. Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol Ther 2003; 8: 284-294.
17. Fittipaldi A, Ferrari A, Zoppe M, Arcangeli C, Pellegrini V, Beltram F, Giacca M. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 tat fusion proteins. J Biol Chem 2003; 278: 34141-34149.
18. Ziegler A, Nervi P, Durrenberger M, Seelig J. The cationic cell-penetrating peptide CPP(TAT) derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: Optical, biophysical, and metabolic evidence. Biochemistry 2005; 44: 138-148.
19. Tunnemann G, Martin RM, Haupt S, Patsch C, Edenhofer F, Cardoso MC. Cargo-dependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells. FASEB J 2006; 20: 1775-1784.
20. Fischer R, Köhler K, Fotin-Mleczek M, Brock R. A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J Biol Chem 2004; 279: 12625-12635.
21. Potocky TB, Menon AK, Gellman SH. Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells. J Biol Chem 2003; 278: 50188-50194.
22. Richard JP, Melikov K, Brooks H, Prevot P, Lebleu B, Chernomordik LV. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J Biol Chem 2005; 280: 15300-15306.
23. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X, Shi Y. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000; 408: 1008-1012.
24. Fotin-Mleczek M, Fischer R, Brock R. Endocytosis and cationic cell-penetrating peptides - a merger of concepts and methods. Curr Pharm Des 2005; 11: 3613-3628.
25. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/ TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8: 808-815.
26. Arnt CR, Chiorean MV, Heldebrant MP, Gores GJ, Kaufmann SH. Synthetic Smac/DIABOLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ. J Biol Chem 2002; 277: 44236-44234.
27. Torgerson TR, Colosia AD, Donahue JP, Lin Y-Z, Hawiger J. Regulation of NF-kappa B, AP-1, NFAT, and STAT1 nuclear import in T lymphocytes by noninvasive delivery of peptide carrying the nuclear localization sequence of NF-kappa B p50. J Immunol 1998; 161: 6084-6092.
28. Borsello T, Clarke PGH, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 2003; 9: 1180-1186.
29. Säälik P, Elmquist A, Hansen M, Padari K, Saar K, Viht K, Langel Ü, Pooga M. Protein cargo delivery properties of cell-penetrating peptides. A comparative study. Bioconjug Chem 2004; 15: 1246-1253.
30. Subtil A, Hemar A, Dautry-Varsat A. Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J Cell Sci 1994; 107: 3461-3468.
31. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 1989; 109: 2731-2739.
32. Keller P, Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J Cell Biol 1998; 140: 1357-1367.
33. Fretz M, Jin J, Conibere R, Penning NA, Al Taei S, Storm G, Futaki S, Takeuchi T, Nakase I, Jones AT. Effects of Na+/H+ exchanger inhibitors on subcellular localisation of endocytic organelles and intracellular dynamics of protein transduction domains HIV-TAT peptide and octaarginine. J Control Release 2006; 116: 247-254.
34. Kielholz P, Labhardt F. Treatment of mental disorders with chlorpromazine. J Clin Exp Psychopathol 1956; 17: 38-44.
35. Seeman P. Atypical antipsychotics: Mechanism of action. Can J Psychiatry 2002; 47: 27-38.
36. Marshak DR, Lukas TJ, Watterson DM. Drug-protein interactions: Binding of chlorpromazine to calmodulin, calmodulin fragments, and related calcium binding proteins. Biochemistry 1985; 24: 144-150.
37. Lippincott-Schwartz J, Altan-Bonnet N, Patterson GH. Photobleaching and photoactivation: Following protein dynamics in living cells. Nat Cell Biol 2003; 5 (Suppl.): S7-S14.
38. van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 1993; 122: 553-563.
39. Henley JR, Krueger EW, Oswald BJ, McNiven MA. Dynamin-mediated internalization of caveolae. J Cell Biol 1998; 141: 85-99.
40. Argyris EG, Kulkosky J, Meyer ME, Xu Y, Mukhtar M, Pomerantz RJ, Williams KJ. The perlecan heparan sulfate proteoglycan mediates cellular uptake of HIV-1 Tat through a pathway responsible for biological activity. Virology 2004; 330: 481-486.
41. Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 2001; 276: 3254-3261.
42. Rusnati M, Coltrini D, Oreste P, Zoppetti G, Albini A, Noonan D, d'Adda di Fagagna F, Giacca M, Presta M. Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size. J Biol Chem 1997; 272: 11313-11320.
43. Goncalves E, Kitas E, Seelig J. Binding of oligoarginine to membrane lipids and heparan sulfate: Structural and thermodynamic characterization of a cell-penetrating peptide. Biochemistry 2005; 44: 2692-2702.
44. Wang LH, Rothberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 1993; 123: 1107-1117.
45. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000; 351: 95-105.
46. van Dam EM, Ten Broeke T, Jansen K, Spijkers P, Stoorvogel W. Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 2002; 277: 48876-48883.
47. Hunyady L, Baukal AJ, Gaborik Z, Olivares-Reyes JA, Bor M, Szaszak M, Lodge R, Catt KJ, Balla T. Differential PI 3-kinase dependence of early and late phases of recycling of the internalized AT1 angiotensin receptor. J Cell Biol 2002; 157: 1211-1222.
48. Gschwendt M, Muller HJ, Kielbassa K, Zang R, Kittstein W, Rincke G, Marks F. Rottlerin, a novel protein kinase inhibitor. Biochem Biophys Res Commun 1994; 199: 93-98.
49. Fischer R, Bächle D, Fotin-Mleczek M, Jung G, Kalbacher H, Brock R. A targeted protease substrate for a quantitative determination of proteolytic activities in the endolysosomal pathway. Chembiochem 2006; 7: 1428-1434.
50. Fotin-Mleczek M, Welte S, Mader O, Duchardt F, Fischer R, Hufnagel H, Scheurich P, Brock R. Cationic cell-penetrating peptides interfere with TNF signaling by induction of TNF receptor internalization. J Cell Sci 2005; 118: 3339-3351.
51. Praefcke GJ, McMahon HT. The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5: 133-147.
52. Silhol M, Tyagi M, Giacca M, Lebleu B, Vives E. Different mechanisms for cellular internalization of the HIV-1 Tat-derived cell penetrating peptide and recombinant proteins fused to Tat. Eur J Biochem 2002; 269: 494-501.
53. Fuchs SM, Raines RT. Pathway for polyarginine entry into mammalian cells. Biochemistry 2004; 43: 2438-2444.
54. Rothbard JB, Jessop TC, Lewis RS, Murray BA, Wender PA. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J Am Chem Soc 2004; 126: 9506-9507.
55. van Kuppevelt TH, Dennissen MA, van Venrooij WJ, Hoet RM, Veerkamp JH. Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney. J Biol Chem 1998; 273: 12960-12966.
56. Fischer R, Mader O, Jung G, Brock R. Extending the applicability of carboxyfluorescein in solid-phase synthesis. Bioconjug Chem 2003; 14: 653-660.