Endocytosis and cationic cell-penetrating peptides - A merger of concepts and methods

Current Pharmaceutical Design

Volumn 11, Issue 28, 2005, Pages 3613-3628

  Fotin Mleczek, M ^a   Fischer, R ^a   Brock, Roland ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Antennapedia homeodomain; Arginine rich peptides; Endocytosis; Fluorescence; Fluorescent proteins; Inhibitors; Tat

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMILORIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BESTATIN; BREFELDIN A; CALPASTATIN; CARRIER PROTEIN; CAVEOLIN 1; CELL PENETRATING PEPTIDE; CHLOROQUINE; CHLORPROMAZINE; CLATHRIN; CYTOCHALASIN D; DEXTRAN; DYNAMIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FURIN; GREEN FLUORESCENT PROTEIN; GROWTH HORMONE RECEPTOR; LACTACYSTIN; LOW DENSITY LIPOPROTEIN; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; NYSTATIN; PROTEINASE; SODIUM PROTON EXCHANGE PROTEIN; SPHINGOLIPID; TRANSACTIVATOR PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; WORTMANNIN;

ACIDIFICATION; CAVEOLA; CELL FRACTIONATION; CELL FREE SYSTEM; CELL LINE; CELL MEMBRANE; CELL SELECTION; CELL TRANSPORT; DRUG DESIGN; DRUG TARGETING; ENDOCYTOSIS; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE MICROSCOPY; GENE DELIVERY SYSTEM; HELA CELL; HUMAN; IN VITRO STUDY; INTRACELLULAR TRANSPORT; ISOTOPE LABELING; LIPID RAFT; MEMBRANE TRANSPORT; NONVIRAL GENE DELIVERY SYSTEM; PHAGOCYTOSIS; PINOCYTOSIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; TRANSPORT VESICLE;

ANIMALS; ENDOCYTOSIS; HUMANS; PEPTIDE HYDROLASES; PEPTIDES; PROTEINS;

EID: 27744528180     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161205774580778     Document Type: Review

References (151)

1. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001; 46: 3-26.
2. Johannes L, Lamaze C. Clathrin-dependent or not: Is it still the question? Traffic 2002; 3: 443-51.
3. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004; 5: 121-32.
4. Dimitrov DS. Virus entry: Molecular mechanism and biomedical applications. Nat Rev Microbiol 2004; 2: 109-22.
5. Sandvig K, van Deurs B. Entry of ricin and Ship toxin into cells: molecular mechanisms and medical perspectives. EMBO J 2000; 9: 5943-50.
6. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55: 1189-93.
7. Joliot A, Pernelle C, Deagostini-Bazin H, Prochiantz A. Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci USA 1991; 88: 1864-8.
8. 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.
9. 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: 16010-7.
10. Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, Ueda K, et al. Arginine-rich peptides. J Biol Chem 2001; 276: 5836-40.
11. Thoren PEG, Persson D, Karlsson M, Norden B. The antennapedia peptide penetratin translocates across lipid bilayers - the first direct observation. FEBS Lett 2000; 482: 265-8.
12. Dietz GPH, Bähr M. Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol Cell Neurosci 2004; 27: 85-131.
13. Fernandez-Carneado J, Kogan MJ, Castel S, Giralt E. Potential peptide carriers: amphipathic proline-rich peptides derived from the N-terminal domain of gammia-zein. Angew Chem Int Ed Engl 2004; 43: 1811-4.
14. Fischer PM, Krausz E, Lane DP. Cellular delivery of impermeable effector molecules in the form of conjugates with peptides capable of mediating membrane translocation. Bioconjugate Chem 2001; 12: 825-41.
15. Futaki S. Arginine-rich peptides: potential for intracellular delivery of macromolecules and the mystery of the translocation mechanisms. Int J Pharm 2002; 245: 1-7.
16. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003; 422: 37-44.
17. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 2002; 13: 238-50.
18. Verkade P, Harder T, Lafont F, Simons K. Induction of caveolae in the apical plasma membrano-of-Madin-Darby canine kidney cells. J Cell Biol 2000; 148: 727-39.
19. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1: 31-9.
20. Harder T, Scheiffele P, Verkade P, Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 1998; 141: 929-42.
21. Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, Brown DA. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem 1999; 274: 3910-7.
22. Liu J, Oh P, Horner T, Rogers RA, Schnitzer JE. Organized endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J Biol Chem 1997; 272: 7211-22.
23. Sowa G, Pypaert M, Sessa WC. Distinction between signaling mechanisms in lipid rafts vs. caveolae, Proc Nad Acad Sci USA 2001; 98: 14072-7.
24. Gaidarov I, Santini F, Warren RA, Keen JH. Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1999; 1: 1-7.
25. Amyere M, Payrastre B, Krause U, Van Der SP, Veithen A, Courtoy PJ. Constitutive macropinocytosis in onicogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol Biol Cell 2000; 11: 3453-67.
26. Schmid SL. Clathrin-coated vesicle formation and protein sorting; an integrated process. Annu Rev Biochem 1997; 66.511-48.
27. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 2001; 17: 517-68.
28. Kirchhausen T. Clathrin. Annu Rev Biochem 2000; 69: 609-727.
29. Robinson MS, Bonifacino JS. Adaptor-related proteins. Curr Opin Cell Biol 2001; 13: 444-53,
30. Parton RG, Richards AA. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 2003; 4: 724-38.
31. Palade GE. Fine structure of blood capillaries. J Appl Phys 1953; 24:1424.
32. Yamada E. The fine structure of the renal glomerulus of the mouse. J Biophys Biochem Cytol 1955; 1: 551-66.
33. Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 2003; 161: 673-7.
34. Rothberg GE, Heuse, JE, Donzell WC,, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992; 68: 673-82.
35. Pelkinans L, Puntener D, Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002; 296: 535-9.
36. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569-72.
37. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001; 293: 2449-52.
38. Nichols BJ, Lippincott-Schwartz J. Endocytosis without clathrin coats. Trends Cell Biol 2001; 11: 406-12.
39. Duncan MJ, Shin JS, Abraham SN. Microbial entry through caveolae: variations on a theme. Cell Microbiol 2002; 4: 783-91.
40. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. Interteukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 2001; 7:661-71.
41. Gruenberg J. The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2001; 2: 721-30.
42. Hewlett LJ, Prescott AR, Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 1994; 124: 689-703.
43. Pelkmans L, Burli T, Zerial M, Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic, Cell 2004; 119: 767-90.
44. Lord JM, Roberts LM. Toxin entry: retrograde transport through the secretory pathway. J Cell Biol 1998; 140: 733-6.
45. Matlack KES, Mothes W, Rapoport TA. Protein translocation: Tunnel vision. Cell 1998; 92: 381-90.
46. Brugidou J, Legrand C, Mery J, Rabie A. The retro-inverso form of a homeobox-derived short peptide is rapidly internalised by cultured neurones: a new basis for an efficient intracellular delivery system. Biochem Biophys Res Commun 1995; 214: 685-93.
47. 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: 50188-94.
48. Rueping M, Mahajan Y, Sauer M, Seebwh D. Cellular uptake studies with beta-peptides. Chembiochem 2002; 3: 257-9.
49. Wender PA, Mitchell DJ, Pattabiraman K, Pelkey ET, Steinman L, Rothbard JB. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc Natl Acad Sci USA 2000; 97: 13003-8.
50. Pietersz GA, Li W, Apostolopoulos V. A 16-mer peptide (RQIKIWFQNRRMKWKK) from antennapedia preferentially targets the class I pathway. Vaccine 2001; 19: 1397-405.
51. Geier E, Pfeifer G, Wilm M, Lucchiari-Hartz M, Baumeister W, Eichmann K, et al. A giant protease with potential to substitute for some functions of the proteasome. Science 1999; 283: 978-81.
52. Rock KL, York IA, Goldberg AL. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat Immunol 2004; 5: 670-7.
53. Seifert U, Maranon C, Shmueli A, Desoutter JF, Wesoloski L, Janek K, et al. An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 2003; 4: 375-9.
54. Stoltze L, Schirle M, Schwarz G, Schroter C, Thompson MW, Hersh LB, et al. Two new proteases in the MHC class I processing pathway. Nat Immunol 2000; 1: 413-8.
55. Saric T, Beninga J, Graef CI, Akopian TN, Rock KL, Goldberg AL. Major histocompatibility complex class I-presented antigenic. peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J Biol Chem 2001; 276: 36474-81.
56. Taylor A. Aminopeptidases: structure and function. FASEB J 1993; 7: 290-8.
57. Pillay CS, Elliott E, Dennison C. Endolysosomal proteolysis and its regulation. Biochem J 2002; 363: 417-29.
58. Lu J, Wertstein PJ, Higashimoto Y, Appella E, Celis E. TAP-independent presentation of CTL epitopes by trojan antigens. J Immunol 2001; 166: 7063-71.
59. Nakayama K. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 1997; 327: 635.
60. Tikhonov I, Ruckwardt TJ, Berg S, Hatfield GS, David PC. Furin cleavage of the HIV-1 Tat protein. FEBS Left 2004; 565: 89-92.
61. Cameron A, Appel J, Houghten RA, Lindberg I. Polyarginines are potent furin inhibitors. J Biol Chem 2000; 275: 36741-9.
62. Kacprzak MM, Peinado JR, Than ME, Appel J, Henrich S, Lipkind G, et al. Inhibition of furin by polyarginine-containing peptides: nanomolar inhibition by nona-D-arginine, J Biol Chem 2004; 279: 36788-94.
63. Serwold T, Gaw S, Shastri N. ER arninopeptidases generate a unique pool of peptides for MHC class I molecules. Nat Immunol 2001; 2: 644-51.
64. Säälik P, Elmquist A, Hansen M, Padari K, Saar K, Viht K, et al. Protein cargo delivery properties of cell-penetrating peptides. A comparative study. Bioconjugate Chem 2004; 15(6): 1246-53.
65. 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: 2347-60.
66. Lippincott-Schwartz J, Snapp E, Kenworthy A. Studying protein dynamics in living cells. Nature Rev Mol Cell Biol 2001; 2: 445-56.
67. Thomas CF, White JG. Four-dimensional imaging: the exploration of space and time. Trends Biotech 1998; 16: 175-82.
68. Fischer R, Waizenegger T, Köhler K, Brock R. A quantitatitive validation of fluorophore-labelled cell-permeable peptide conjugates: Fluorophore and cargo dependence of import. Biochim Biophys Acta 2002; 1564: 365-74.
69. Waizenegger T, Fischer R, Brock R. Intracellular concentration measurements in adherent cells: A comparison of import efficiencies of cell-permeable peptides. Biol Chem 2002; 383: 291-9.
70. Zaro JL, Shen WC. Quantitative comparison of membrane transduction and endocytosis of oligopeptides. Biochem Biophys Res Common 2003; 307: 241-7.
71. Elmquist A, Laniel Ü. In vitro uptake and stability study of pVEC and its all-D analog. Biol Chem 2003; 384: 387-93.
72. 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: 12625-35.
73. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, et al. Cell-penetrating peptides: A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003; 278: 585-90.
74. Smart EJ, Ying YS, Conrad PA, Anderson RG. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J Cell Biol 1994; 127: 1185-97.
75. Orlandi PA, Fishman PH. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 1998; 141: 905-15.
76. Pike LJ, Casey L. Cholesterol levels modulate EGF receptor-mediated signaling by altering receptor function and trafficking. Biochemistry 2002; 41: 10315-22.
77. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999; 10: 961-74.
78. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA 1999; 96: 6775-80.
79. Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol 1994; 127: 1199-215.
80. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 1989; 109: 2731-9.
81. Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, et al. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 2002; 158: 1119-31.
82. Araki N, Johnson MT, Swanson JA. A role for phosphomositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 1996; 13 5: 1249-60.
83. Arayere M, Mettlen K Van Der SP, Platek A, Payrastre B, Veithen A, et al. Origin, originality, functions, subversions; and molecular signalling of macropinocytosis. Int J Med Microbiol 2002; 291: 487-94.
84. Li G, D'Souza-Schorey C, Barbieri MA, Roberts RL, Ktippel A, Williams LT, et al Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc Natl Acad Sci USA 1995; 92: 10207-11.
85. Spiro DJ, Boll W, Kirchhausen T, Wessling-Resnick M. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol Biol Cell 1996; 7: 355-67.
86. Traub LM. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol 2003; 163: 203-8.
87. 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: 3461-8.
88. 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: 1107-17.
89. Sandvig K, Olsnes S, Petersen OW, van Deurs B. Acidification of the cytosol inhibits endocytosis from coated pits. J Cell Biol 1987; 105: 679-89.
90. Heuser JE, Anderson RG. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 1989; 108: 389-400.
91. Moss AL, Ward WF. Multiple pathways for ligand internalization in rat hepatocytes. I: Effects of anoxia, phenylarsine oxide and monensin. J Cell Physiol 199 1; 149: 313-8.
92. Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 1988; 85: 7972-6.
93. Clague MJ, Urbe S, Aniento F, Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 1994; 269: 21-4.
94. Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 1991; 67: 601-16.
95. Reaves B, Banting G. Perturbation of the morphology of the trans-Golgi network following Brefeldin A treatment: redistribution of a TGN-specific integral membrane protein, TGN38. J Cell Biol 1992; 116: 85-94.
96. van Dam EM, Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell 2002; 13: 169-82.
97. Drecktrah D, de Figueiredo P, Mason RM, Brown WJ. Retrograde trafficking of both Golgi complex and TON markers to the ER induced by nordihydroguaiaretic acid and cyclofenil diphenol. J Cell Sci 1998; 111: 951-65.
98. Kessler BM, Glas R, Ploegh HL. MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation. Mol Immunol 2002; 39: 171-9.
99. Kisselev AF, Goldberg AL. Proteasome inhibitors: from research tools to drug candidates. Chem Biol 2001; 8: 739-58.
100. Steer D, Lew R, Perlmutter P, Smith Al, Aguilar M-I. Inhibitors of metalloendopeptidase EC 3.4.24.15 and EC 3.4.24.16 stabilized by the incorporation of β-amino acids. Biochemistry 2002; 4: 10819-26.
101. York IA, Mo AY, Lemerise K, Zeng W, Shen Y, Abraham CR, et al. The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 2003; 18: 429-40.
102. Vidard L, Rock KL, Benacerraf B. The generation of immunogenic peptides can be selectively increased or decreased by proteolytic enzyme inhibitors. J Immunol 1991; 147: 1786-91.
103. Tamai M, Matsumoto K, Omura S, Koyama I, Ozawa Y, Hanada K. In vitro and in vivo inhibition of cysteine proteinases by EST, a new analog of E-64. J Pharmacobiodyn 1986; 9: 672-7.
104. Katunuma N, Matsunaga Y, Himeno K, Hayashi Y. Insights into the roles of cathepsins in antigen processing and presentation revealed by specific inhibitors. Biol Chem 2003; 384: 883-90.
105. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127: 915-34.
106. Shpetner HS, Vallee RB. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 1989; 59: 421-32.
107. 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: 553-63.
108. Henley JR, Krueger EW, Oswald BJ, McNiven MA. Dynamin-mediated internalization of caveolae. J Cell Biol 1998; 141: 85-99.
109. Benmerah A, Bayrou M, Cerf-Bonsussan N, Dautry-Varsat A. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 1999; 112: 1303-11.
110. Morgan JR, Prasad K, Jin S, Augustine GJ, Lafer EM. Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling. J Biol Chem 2003; 278: 33583-92.
111. Ehrlich M, Boll W, van Oijen A, Hariharan R, Chandran K, Nibert ML, et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004; 118: 591-605.
112. Hanover JA, Beguinot L, Willingham MC, Pastan IH. Transit of receptors for epidermal growth factor and transferrin through clathrin-coated pits. Analysis of the kinetics of receptor entry. J Biol Chem 1985; 260: 15938-45.
113. Hopkins CR, Miller K, Beardmore JM. Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J Cell Sci Suppl 1985; 3: 173-86.
114. Hacker U, Albrecht R, Maniak M. Fluid-phase uptake by macropinocytosis in Dictyostellium. J Cell Sci 1997; 110: 105-12.
115. Pagano RE, Martin OC, Kang HC, Haugland RP. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J Cell Biol 1991; 113:1267-79.
116. Verkhusha VV, Lukyanov KA. The molecular properties and applications of Anthozoa fluorescent proteins and chromoproteins. Nat Biotechnol 2004; 22: 289-96.
117. Zhang J, Campbell RE, Ting AY, Tsien RY. Creating new fluorescent probes for cell biology. Nat Rev Mol Cell Biol 2002; 3: 906-18.
118. 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: 284-94.
119. Henry RM, Hoppe AD, Joshi N, Swanson JA. The uniformity of phagosome maturation in macrophages. J Cell Biol 2004; 164: 185-94.
120. Waguri S, Dewitte F, Le Borgne R, Rouille Y, Uchiyama Y, Dubremetz JF, et al. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol Biol Cell 2003; 14: 142-55.
121. Sonnichsen B, de Renzis S, Nielsen E, Rictdorf J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rabl1. J Cell Biol 2000; 149: 901-14.
122. Pfeffer S, Aivazian D. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 2004; 5: 886-96.
123. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107-17.
124. Scheller A, Wiesner B, Melzig M, Bienert M, Oehlke J. Evidence for an amphipathicity independent cellular uptake of amphipatic cell-penetrating peptides. Eur J Biochem 2000, 267: 6043-9.
125. Rigler R, Mets Ü, Widengren J, Kask P. Fluorescence correlation spectroscopy with high count rate and low background: Analysis of translational diffusion. Eur Biophys J 1993; 22: 169-75.
126. Elson EL, Madge D. Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers 1974; 13: 1-27.
127. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fitsogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10: 310-5.
128. Drin G, Demene H, Temsamani J, Brasseur R. Translocation of the pAntp peptide and its amphiphatic analogue AP-2AL. Biochemistry 2001; 40: 1824-34.
129. Magzoub M, Eriksson LEG, Gräslund A. Comparison of the interaction, positioning, structure induction and membrane pertubation of cell-penetrating peptides and non-translocating variants with phospholipid vesicles. Biophys Chem 2003; 103: 271-88.
130. Lindberg M, Biverstahl H, Gräslund A, Mäler L, Structure and positioning comparison of two variants of perietratin in two different membrane mimicking systems by NMR. Eur J Biochem 2003; 270: 3055-63.
131. Salamon Z, Lindblom G, Tollin G. Plasmon-waveguide resonance and impedance spectroscopy studies of the interaction between penetratin and supported lipid bilayer membranes. Biophys J 2003; 84: 1796-807.
132. Braftwall CEB, Lincoln P, Norden B. Orientation and conformation of cell-penetrating peptide penetratin in phospholipid vesicle membranes determined by polarized-light spectroscopy. J Am Chem Soc 2003; 125: 14214-5.
133. Bellet-Amalric E, Blaudez D, Desbat B, Graner F, Gauthier F, Renault A. 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 2000; 1467: 131-43.
134. Fragneto G, Graner F, Chariat T, Dubos P, Bellet-Amalric E. Interaction of the third helix of Antennapedia Homoeodomain with a deposited phospholipid bilayer: a neutron reflectivity structural study. Langmuir 2000; 16: 4581-8.
135. 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: 9506-7.
136. Terrone D, Sang SL, Roudaia L, Silvius JR. Penetratin and related cell-penetrating cationic peptides can translocate across lipid bilayers in the presence of a transbilayer potential. Biochemistry 2003; 42: 13787-99.
137. Lundberg M, Johansson M. Is VP22 nuclear homing an artifact? Nat Biotechnol 2001; 19: 713-4.
138. Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 2001; 276: 3254-61.
139. 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: 35109-14.
140. 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: 31192-201.
141. 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.
142. Fittipaldi A, Ferrari A, Zoppe M, Arcangeli C, Pellegrini V, Beltram F, et al. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 tat fusion proteins. J Biol Chem 2003; 278: 34141-43149.
143. Eguchi A, Akuta T, Okuyama H, Senda T, Yokoi H, Inokuchi H, et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem 2001; 276: 26204-10.
144. Elmquist A, Lindgren M, Bartfai T, Langel U. VE-cadherin-derived cell-penetrating peptide, pVEC, with carrier functions. Exp Cell Res 2001; 269: 237-44.
145. Caron NJ, Quenneville SP, Tremblay JP. Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem Biophys Res Commun 2004; 319: 12-20.
146. Sengoku T, Bondada V, Hassane D, Dubal S, Geddes JW. Tat-calpastatin fusion proteins transduce primary rat cortical neurons but do not inhibit cellular calpain activity. Exp Neurol 2004; 188: 161-70.
147. Mader O, Reiner K, Egelhaaf H-J, Fischer R, Brock R. Structure property analysis of pentamethine indocyanine dyes: Identification of a new dye for life science applications, Bioconjugate Chem 2004; 15: 70-8.
148. Wachsmuth M, Waldeck W, Langowski J. Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J Mol Biol 2000; 298: 677-89.
149. Kitts DD, Weiler K. Bioactive proteins and peptides from food sources. Applications of bioprocesses used in isolation and recovery. Curr Pharm Design 2003; 9(16): 1309-23.
150. Milligan G, Feng GJ, Ward RJ, Sartania N, Ramsay D, McLean AJ, et al. G protein-coupled receptor fusion proteins in drug discovery. Curr Pharm Design 2004; 10(17): 1989-2001.
151. Stefanidakis, M. and Koivunen, E. Peptide-mediated delivery of therapeutic and imaging agents into mammalian cells. Curr Pharm Design 2004; 10(24): 3033-44.