Mechanisms of cellular uptake of cell-penetrating peptides

Journal of Biophysics

Volumn , Issue , 2011, Pages

  Gräslund, Astrid ^a   Madani, Fatemeh ^a   Lindberg, Staffan ^a   Langel, Ülo ^a   Futaki, Shiroh ^b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959365312     PISSN: 16878000     EISSN: 16878019     Source Type: Journal    
DOI: 10.1155/2011/414729     Document Type: Review

References (83)

1. Jrver P., Langel., Cell-penetrating peptidesa brief introduction Biochimica et Biophysica Acta 2006 1758 3 260 263
2. El-Andaloussi S., Holm T., Langel., Cell-penetrating peptides: mechanisms and applications Current Pharmaceutical Design 2005 11 28 3597 3611 (Pubitemid 41630987)
3. Green M., Loewenstein P. M., Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein Cell 1988 55 6 1179 1188 (Pubitemid 19020070)
4. Vivs 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 Journal of Biological Chemistry 1997 272 25 16010 16017 (Pubitemid 27265584)
5. Joliot A., Pernelle C., Deagostini-Bazin H., Prochiantz A., Antennapedia homeobox peptide regulates neural morphogenesis Proceedings of the National Academy of Sciences of the United States of America 1991 88 5 1864 1868 (Pubitemid 21916327)
6. Joliot A. H., Triller A., Volovitch M., Pernelle C., Prochiantz A., -2,8-polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide New Biologist 1991 3 11 1121 1134
7. Derossi D., Joliot A. H., Chassaing G., Prochiantz A., The third helix of the Antennapedia homeodomain translocates through biological membranes Journal of Biological Chemistry 1994 269 14 10444 10450 (Pubitemid 24198241)
8. Derossi D., Calvet S., Trembleau A., Brunissen A., Chassaing G., Prochiantz A., Cell internalization of the third helix of the antennapedia homeodomain is receptor-independent Journal of Biological Chemistry 1996 271 30 18188 18193 (Pubitemid 26250811)
9. Nakase I., Hirose H., Tanaka G., Tadokoro A., Kobayashi S., Takeuchi T., Futaki S., Cell-surface accumulation of flock house virus-derived peptide leads to efficient internalization via macropinocytosis Molecular Therapy 2009 17 11 1868 1876
10. Hessa T., Kim H., Bihlmaier K., Lundin C., Boekel J., Andersson H., Nilsson I., White S. H., Von Heijne G., Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 2005 433 7024 377 381 (Pubitemid 40203311)
11. Futaki S., Suzuki T., Ohashi W., Yagami T., Tanaka S., Ueda K., Sugiura Y., Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery Journal of Biological Chemistry 2001 276 8 5836 5840
12. Thorn P. E. G., Persson D., Isakson P., Goksr M., nfelt A., Nordn B., Uptake of analogs of penetratin, Tat(48-60) and oligoarginine in live cells Biochemical and Biophysical Research Communications 2003 307 1 100 107 (Pubitemid 36808542)
13. Elmquist A., Lindgren M., Bartfai T., Langel., Ve-cadherin-derived cell-penetrating peptide, pVEC with carrier functions Experimental Cell Research 2001 269 2 237 244 (Pubitemid 32907165)
14. El-Andaloussi S., Johansson H. J., Holm T., Langel., A novel cell-penetrating peptide, M918, for efficient delivery of proteins and peptide nucleic acids Molecular Therapy 2007 15 10 1820 1826 (Pubitemid 47434189)
15. Soomets U., Lindgren M., Gallet X., Hllbrink M., Elmquist A., Balaspiri L., Zorko M., Pooga M., Brasseur R., Langel., Deletion analogues of transportan Biochimica et Biophysica Acta 2000 1467 1 165 176 (Pubitemid 30621595)
16. Zorko M., Langel., Cell-penetrating peptides: mechanism and kinetics of cargo delivery Advanced Drug Delivery Reviews 2005 57 4 529 545 (Pubitemid 40255559)
17. Ziegler A., Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans Advanced Drug Delivery Reviews 2008 60 4-5 580 597 (Pubitemid 351215575)
18. Pooga M., Hllbrink M., Zorko M., Langel., Cell penetration by transportan FASEB Journal 1998 12 1 67 77 (Pubitemid 28060272)
19. Magzoub M., Grslund A., Cell-penetrating peptides: from inception to application Quarterly Reviews of Biophysics 2004 37 2 147 195
20. Avrahami D., Shai Y., Bestowing antifungal and antibacterial activities by lipophilic acid conjugation to D,L-amino acid-containing antimicrobial peptides: a plausible mode of action Biochemistry 2003 42 50 14946 14956 (Pubitemid 37553525)
21. Richard J. P., Melikov K., Vives E., Ramos C., Verbeure B., Gait M. J., Chernomordik L. V., Lebleu B., Cell-penetrating peptides: a reevaluation of the mechanism of cellular uptake Journal of Biological Chemistry 2003 278 1 585 590 (Pubitemid 36043612)
22. Wadia J. S., Stan R. V., Dowdy S. F., Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nature Medicine 2004 10 3 310 315 (Pubitemid 38667624)
23. Dominski Z., Kole R., Restoration of correct splicing in thalassemic pre-mRNA by antisense oligonucleotides Proceedings of the National Academy of Sciences of the United States of America 1993 90 18 8673 8677 (Pubitemid 23277732)
24. Kang S. H., Cho M. J., Kole R., Up-regulation of luciferase gene expression with antisense oligonucleotides: implications and applications in functional assay development Biochemistry 1998 37 18 6235 6239 (Pubitemid 28213640)
25. Langel., Cell-Penetrating Peptides: Processes and Applications 2006 2nd Boca Raton, Fla, USA CRC Press
26. Kaplan I. M., Wadia J. S., Dowdy S. F., Erratum: Cationic TAT peptide transduction domain enters cells by macropinocytosis (Journal of Controlled Release (2005) 102 (247253) DOI: 10.1016/j.jconrel.2004.10.018) Journal of Controlled Release 2005 107 3 571 572 (Pubitemid 41393363)
27. Vercauteren D., Vandenbroucke R. E., Jones A. T., Rejman J., Demeester J., De Smedt S. C., Sanders N. N., Braeckmans K., The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls Molecular Therapy 2010 18 3 561 569
28. Sieczkarski S. B., Whittaker G. R., Dissecting virus entry via endocytosis Journal of General Virology 2002 83 7 1535 1545 (Pubitemid 34721298)
29. Sandgren S., Cheng F., Belting M., Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide: role for cell-surface proteoglycans Journal of Biological Chemistry 2002 277 41 38877 38883 (Pubitemid 35157770)
30. Ohkuma S., Poole B., Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents Proceedings of the National Academy of Sciences of the United States of America 1978 75 7 3327 3331 (Pubitemid 8389720)
31. Wibo M., Poole B., Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B Journal of Cell Biology 1974 63 2 430 440
32. Takeuchi T., Kosuge M., Tadokoro A., Sugiura Y., Nishi M., Kawata M., Sakai N., Matile S., Futaki S., Direct and rapid cytosolic delivery using cell-penetrating peptides mediated by pyrenebutyrate ACS Chemical Biology 2006 1 5 299 303
33. Perret F., Nishihara M., Takeuchi T., Futaki S., Lazar A. N., Coleman A. W., Sakai N., Matile S., Anionic fullerenes, calixarenes, coronenes, and pyrenes as activators of oligo/polyarginines in model membranes and live cells Journal of the American Chemical Society 2005 127 4 1114 1115 (Pubitemid 40228679)
34. Sakai N., Takeuchi T., Futaki S., Matile S., Direct observation of anion-mediated translocation of fluorescent oligoarginine carriers into and across bulk liquid and anionic bilayer membranes ChemBioChem 2005 6 1 114 122 (Pubitemid 40128644)
35. Nishihara M., Perret F., Takeuchi T., Futaki S., Lazar A. N., Coleman A. W., Sakai N., Matile S., Arginine magic with new counterions up the sleeve Organic and Biomolecular Chemistry 2005 3 9 1659 1669 (Pubitemid 40683090)
36. Matsuzaki K., Yoneyama S., Murase O., Miyajima K., Transbilayer transport of ions and lipids coupled with mastoparan X translocation Biochemistry 1996 35 25 8450 8456 (Pubitemid 26234950)
37. Pouny Y., Rapaport D., Mor A., Nicolas P., Shai Y., Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes Biochemistry 1992 31 49 12416 12423 (Pubitemid 23163118)
38. Lee M. T., Hung W. C., Chen F. Y., Huang H. W., Many-body effect of antimicrobial peptides: on the correlation between lipid's spontaneous curvature and pore formation Biophysical Journal 2005 89 6 4006 4016 (Pubitemid 41725621)
39. Rothbard J. B., Jessop T. C., Lewis R. S., Murray B. A., Wender P. A., Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells Journal of the American Chemical Society 2004 126 31 9506 9507 (Pubitemid 39031015)
40. Duchardt F., Fotin-Mleczek M., Schwarz H., Fischer R., Brock R., A comprehensive model for the cellular uptake of cationic cell-penetrating peptides Traffic 2007 8 7 848 866 (Pubitemid 46971632)
41. Kosuge M., Takeuchi T., Nakase I., Jones A. T., Futaki S., Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans Bioconjugate Chemistry 2008 19 3 656 664 (Pubitemid 351431397)
42. Deshayes S., Morris M. C., Divita G., Heitz F., Interactions of amphipathic CPPs with model membranes Biochimica et Biophysica Acta 2006 1758 3 328 335
43. Derossi D., Chassaing G., Prochiantz A., Trojan peptides: the penetratin system for intracellular delivery Trends in Cell Biology 1998 8 2 84 87 (Pubitemid 28056816)
44. Jones A. T., Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides Journal of Cellular and Molecular Medicine 2007 11 4 670 684 (Pubitemid 47313298)
45. Mayor S., Pagano R. E., Pathways of clathrin-independent endocytosis Nature Reviews Molecular Cell Biology 2007 8 8 603 612 (Pubitemid 47106613)
46. Lundberg M., Johansson M., Is VP22 nuclear homing an artifact? Nature Biotechnology 2001 19 8 713 714
47. Mitchell D. J., Steinman L., Kim D. T., Fathman C. G., Rothbard J. B., Polyarginine enters cells more efficiently than other polycationic homopolymers Journal of Peptide Research 2000 56 5 318 325
48. Elmquist A., Hansen M., Langel., Structure-activity relationship study of the cell-penetrating peptide pVEC Biochimica et Biophysica Acta 2006 1758 6 721 729 (Pubitemid 44080079)
49. Thorn P. E. G., Persson D., Esbjrner E. K., Goksr M., Lincoln P., Nordn B., Membrane binding and translocation of cell-penetrating peptides Biochemistry 2004 43 12 3471 3489 (Pubitemid 38391703)
50. Wender P. A., Mitchell D. J., Pattabiraman K., Pelkey E. T., Steinman L., Rothbard J. B., The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters Proceedings of the National Academy of Sciences of the United States of America 2000 97 24 13003 13008
51. Mueller J., Kretzschmar I., Volkmer R., Boisguerin P., Comparison of cellular uptake using 22 CPPs in 4 different cell lines Bioconjugate Chemistry 2008 19 12 2363 2374
52. Tnnemann G., Martin R. M., Haupt S., Patsch C., Edenhofer F., Cardoso M. C., Cargo-dependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells FASEB Journal 2006 20 11 1775 1784 (Pubitemid 44933791)
53. Fischer R., Waizenegger T., Khler K., Brock R., A quantitative validation of fluorophore-labelled cell-permeable peptide conjugates: fluorophore and cargo dependence of import Biochimica et Biophysica Acta 2002 1564 2 365 374
54. Lundberg P., El-Andaloussi S., Stl T., Johansson H., Langel., Delivery of short interfering RNA using endosomolytic cell-penetrating peptides FASEB Journal 2007 21 11 2664 2671 (Pubitemid 47372734)
55. Dietz G. P. H., Bhr M., Delivery of bioactive molecules into the cell: the Trojan horse approach Molecular and Cellular Neuroscience 2004 27 2 85 131 (Pubitemid 39370094)
56. Guterstam P., Madani F., Hirose H., Takeuchi T., Futaki S., EL Andaloussi S., Grslund A., Langel., Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate Biochimica et Biophysica Acta 2009 1788 12 2509 2517
57. Slik P., Elmquist A., Hansen M., Padari K., Saar K., Viht K., Langel., Pooga M., Protein cargo delivery properties of cell-penetrating peptides. A comparative study Bioconjugate Chemistry 2004 15 6 1246 1253 (Pubitemid 39552013)
58. Richard J. P., Melikov K., Brooks H., Prevot P., Lebleu B., Chernomordik L. V., Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors Journal of Biological Chemistry 2005 280 15 15300 15306 (Pubitemid 40562886)
59. Fittipaldi A., Ferrari A., Zopp M., Arcangeli C., Pellegrini V., Beltram F., Giacca M., Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins Journal of Biological Chemistry 2003 278 36 34141 34149 (Pubitemid 37553255)
60. Nakase I., Niwa M., Takeuchi T., Sonomura K., Kawabata N., Koike Y., Takehashi M., Tanaka S., Ueda K., Simpson J. C., Jones A. T., Sugiura Y., Futaki S., Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement Molecular Therapy 2004 10 6 1011 1022 (Pubitemid 39625245)
61. El-Andaloussi S., Johansson H. J., Lundberg P., Langel., Induction of splice correction by cell-penetrating peptide nucleic acids Journal of Gene Medicine 2006 8 10 1262 1273 (Pubitemid 44660525)
62. Tyagi M., Rusnati M., Presta M., Giacca M., Internalization of HIV-1 Tat requires cell surface heparan sulfate proteoglycans Journal of Biological Chemistry 2001 276 5 3254 3261
63. Ishihara M., Heparan sulfate proteoglycans are receptors for extracellular HIV-1 Tat internalization Trends in Glycoscience and Glycotechnology 2001 13 72 433 434
64. Rusnati M., Tulipano G., Urbinati C., Tanghetti E., Giuliani R., Giacca M., Ciomei M., Corallini A., Presta M., The basic domain in HIV-1 tat protein as a target for polysulfonated heparin-mimicking extracellular Tat antagonists Journal of Biological Chemistry 1998 273 26 16027 16037 (Pubitemid 28311370)
65. Padari K., Slik P., Hansen M., Koppel K., Raid R., Langel., Pooga M., Cell transduction pathways of transportans Bioconjugate Chemistry 2005 16 6 1399 1410 (Pubitemid 41681506)
66. Brny-Wallje E., Gaur J., Lundberg P., Langel., Grslund A., Differential membrane perturbation caused by the cell penetrating peptide Tp10 depending on attached cargo FEBS Letters 2007 581 13 2389 2393 (Pubitemid 46764694)
67. Marinova Z., Vukojevi V., Surcheva S., Yakovleva T., Cebers G., Pasikova N., Usynin I., Hugonin L., Fang W., Hallberg M., Hirschberg D., Bergman T., Langel., Hauser K. F., Pramanik A., Aldrich J. V., Grslund A., Terenius L., Bakalkin G., Translocation of dynorphin neuropeptides across the plasma membrane: a putative mechanism of signal transmission Journal of Biological Chemistry 2005 280 28 26360 26370 (Pubitemid 41022234)
68. Chavkin C., James I. F., Goldstein A., Dynorphin is a specific endogenous ligand of the opioid receptor Science 1982 215 4531 413 415 (Pubitemid 12132127)
69. Kuzmin A., Madjid N., Terenius L., gren S. O., Bakalkin G., Big dynorphin, a prodynorphin-derived peptide produces NMDA receptor-mediated effects on memory, anxiolytic-like and locomotor behavior in mice Neuropsychopharmacology 2006 31 9 1928 1937
70. Prusiner S. B., Prions Proceedings of the National Academy of Sciences of the United States of America 1998 95 23 13363 13383 (Pubitemid 28525623)
71. Magzoub M., Sandgren S., Lundberg P., Oglecka K., Lilja J., Wittrup A., Gran Eriksson L. E., Langel., Belting M., Grslund A., N-terminal peptides from unprocessed prion proteins enter cells by macropinocytosis Biochemical and Biophysical Research Communications 2006 348 2 379 385 (Pubitemid 44188583)
72. Lfgren K., Wahlstrm A., Lundberg P., Langel., Grslund A., Bedecs K., Antiprion properties of prion protein-derived cell-penetrating peptides FASEB Journal 2008 22 7 2177 2184 (Pubitemid 351948637)
73. Lande R., Gregorio J., Facchinetti V., Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide Nature 2007 449 7162 564 569 (Pubitemid 47525141)
74. Sandgren S., Wittrup A., Cheng F., Jnsson M., Eklund E., Busch S., Belting M., The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis Journal of Biological Chemistry 2004 279 17 17951 17956 (Pubitemid 38568102)
75. Zhang X., Oglcka K., Sandgren S., Belting M., Esbjrner E. K., Nordn B., Grslund A., Dual functions of the human antimicrobial peptide LL-37-target membrane perturbation and host cell cargo delivery Biochimica et Biophysica Acta 2010 1798 12 2201 2208
76. Yeaman M. R., Yount N. Y., Mechanisms of antimicrobial peptide action and resistance Pharmacological Reviews 2003 55 1 27 55 (Pubitemid 36268398)
77. Izadpanah A., Gallo R. L., Antimicrobial peptides Journal of the American Academy of Dermatology 2005 52 3 381 392
78. Almeida P. F., Pokorny A., Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics Biochemistry 2009 48 34 8083 8093
79. Console S., Marty C., Garca-Echeverra C., Schwendener R., Ballmer-Hofer K., Antennapedia and HIV transactivator of transcription (TAT) "protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans Journal of Biological Chemistry 2003 278 37 35109 35114 (Pubitemid 37102274)
80. Wade D., Boman A., Wahlin B., Drain C. M., Andreu D., Boman H. G., Merrifield R. B., All-D amino acid-containing channel-forming antibiotic peptides Proceedings of the National Academy of Sciences of the United States of America 1990 87 12 4761 4765
81. Shai Y., Mode of action of membrane active antimicrobial peptides Biopolymers 2002 66 4 236 248 (Pubitemid 36098316)
82. Nekhotiaeva N., Elmquist A., Rajarao G. K., Hllbrink M., Langel., Good L., Cell entry and antimicrobial properties of eukaryotic cell-penetrating peptides FASEB Journal 2004 18 2 394 396
83. Henriques S. T., Melo M. N., Castanho M. A. R. B., Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochemical Journal 2006 399 1 1 7 (Pubitemid 44505401)