Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides

Advanced Drug Delivery Reviews

Volumn 60, Issue 4-5, 2008, Pages 598-607

  Nakase, Ikuhiko ^a   Takeuchi, Toshihide ^a   Tanaka, Gen ^b   Futaki, Shiroh ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Arginine rich peptide; Counter anion; Endocytosis; Macropinocytosis; Membrane translocation; Membrane permeable peptide; Non endocytic uptake

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; DRUG DELIVERY;

ARGININE-RICH PEPTIDES; BIOACTIVE MOLECULES; ENDOCYTOSIS; MACROPINOCYTOSIS; MEMBRANE-PERMEABLE PEPTIDE;

PEPTIDES;

ARGININE; CELL PENETRATING PEPTIDE; GUANIDINE DERIVATIVE;

ENDOCYTOSIS; INTERNALIZATION; MEMBRANE PERMEABILITY; PRIORITY JOURNAL; REVIEW;

ARGININE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DRUG CARRIERS; ENDOCYTOSIS; HUMANS; METHODS; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PEPTIDES;

EID: 38949188925     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2007.10.006     Document Type: Review

References (89)

1. Joliot A., and Prochiantz A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 6 (2004) 189-196
2. Futaki S. Oligoarginine vectors for intracellular delivery: design and cellular-uptake mechanisms. Biopolymers 84 (2006) 241-249
3. Gupta B., and Torchilin V.P. Transactivating transcriptional activator-mediated drug delivery. Expert Opin. Drug Deliv. 3 (2006) 177-190
4. Goun E.A., Pillow T.H., Jones L.R., Rothbard J.B., and Wender P.A. Molecular transporters: synthesis of oligoguanidinium transporters and their application to drug delivery and real-time imaging. Chembiochem 7 (2006) 1497-1515
5. Snyder E.L., and Dowdy S.F. Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin. Drug Deliv. 2 (2005) 43-51
6. In: Langel Ü. (Ed). Handbook of Cell-Penetrating Peptides. Second Edition (2006), CRC Press, Boca Raton
7. In: Torchilin V.P. (Ed). Special theme issue on Protein-and peptide-mediated transduction: Mechanisms and implications for drug delivery. Adv. Drug Deliv. Rev vol. 57 (2005) 487-665 Issue 4
8. Vivès E., Brodin P., and 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. 272 (1997) 16010-16017
9. Rothbard J.B., Garlington S., Lin Q., Kirschberg T., Kreider E., McGrane P.L., Wender P.A., and Khavari P.A. Conjugation of arginine oligomers to cyclosporin A facilitates topical delivery and inhibition of inflammation. Nat. Med. 6 (2000) 1253-1257
10. Futaki S., Suzuki T., Ohashi W., Yagami T., Tanaka S., Ueda K., and Sugiura Y. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276 (2001) 5836-5840
11. Rothbard J.B., Jessop T.C., Lewis R.S., Murray B.A., and Wender P.A. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J. Am. Chem. Soc. 126 (2004) 9506-9507
12. Sakai N., Takeuchi T., Futaki S., and Matile S. Direct observation of anion-mediated translocation of fluorescent oligoarginine carriers into and across bulk liquid and anionic bilayer membranes. Chembiochem 6 (2005) 114-122
13. Richard J.P., Melikov K., Vivès E., Ramos C., Verbeure B., Gait M.J., Chernomordik L.V., and Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278 (2003) 585-590
14. Richard J.P., Melikov K., Brooks H., Prevot P., Lebleu B., and Chernomordik L.V. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem. 280 (2005) 15300-15306
15. 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., and Futaki S. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol. Ther. 10 (2004) 1011-1022
16. Suzuki T., Futaki S., Niwa M., Tanaka S., Ueda K., and Sugiura Y. Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 277 (2002) 2437-2443
17. Console S., Marty C., García-Echeverría C., Schwendener R., and 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. J. Biol. Chem. 278 (2003) 35109-35114
18. Ziegler A., and Seelig J. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters. Biophys. J. 86 (2004) 254-263
19. Goncalves E., Kitas E., and Seelig J. Binding of oligoarginine to membrane lipids and heparan sulfate: structural and thermodynamic characterization of a cell-penetrating peptide. Biochemistry 44 (2005) 2692-2702
20. Fuchs S.M., and Raines R.T. Pathway for polyarginine entry into mammalian cells. Biochemistry 43 (2004) 2438-2444
21. Wadia J.S., Stan R.V., and Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10 (2004) 310-315
22. Kaplan I.M., Wadia J.S., and Dowdy S.F. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control. Release 102 (2005) 247-253
23. + exchanger inhibitors on subcellular localisation of endocytic organelles and intracellular dynamics of protein transduction domains HIV-TAT peptide and octaarginine. J. Control. Release 116 (2006) 247-254
24. Nakase I., Tadokoro A., Kawabata N., Takeuchi T., Katoh H., Hiramoto K., Negishi M., Nomizu M., Sugiura Y., and Futaki S. Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 46 (2007) 492-501
25. Futaki S., Nakase I., Tadokoro A., Takeuchi T., and Jones A.T. Arginine-rich peptides and their internalization mechanisms. Biochem. Soc. Trans. 35 (2007) 784-787
26. A. T. Jones, Macropinocytosis: searching for an endocytic identity and a role in the uptake of cell penetrating peptides, J. Cell. Mol. Med. 11 (2007) 670-684.
27. Conner S.D., and Schmid S.L. Regulated portals of entry into the cell. Nature 422 (2003) 37-44
28. Frankel A.D., and Pabo C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55 (1988) 1189-1193
29. Green M., and Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55 (1988) 1179-1188
30. Frankel A.D., and Young J.A. HIV-1: fifteen proteins and an RNA. Annu. Rev. Biochem. 67 (1998) 1-25
31. Fawell S., Seery J., Daikh Y., Moore C., Chen L.L., Pepinsky B., and Barsoum J. Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 664-668
32. Nagahara H., Vocero-Akbani A.M., Snyder E.L., Ho A., Latham D.G., Lissy N.A., Becker-Hapak M., Ezhevsky S.A., and Dowdy S.F. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4 (1998) 1449-1452
33. Vocero-Akbani A.M., Heyden N.V., Lissy N.A., Ratner L., and Dowdy S.F. Killing HIV-infected cells by transduction with an HIV protease-activated caspase-3 protein. Nat. Med. 5 (1999) 29-33
34. Schwarze S.R., Ho A., Vocero-Akbani A., and Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285 (1999) 1569-1572
35. Futaki S., Goto S., Suzuki T., Nakase I., and Sugiura Y. Structural variety of membrane permeable peptides. Curr. Protein Pept. Sci. 4 (2003) 87-96
36. Futaki S., Goto S., and Sugiura Y. Membrane permeability commonly shared among arginine-rich peptides. J. Mol. Recognit. 16 (2003) 260-264
37. Rothbard J.B., Kreider E., VanDeusen C.L., Wright L., Wylie B.L., and Wender P.A. Arginine-rich molecular transporters for drug delivery: role of backbone spacing in cellular uptake. J. Med. Chem. 45 (2002) 3612-3618
38. Ferrari A., Pellegrini V., Arcangeli C., Fittipaldi A., Giacca M., and Beltram F. Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol. Ther. 8 (2003) 284-294
39. Derossi D., Joliot A.H., Chassaing G., and Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269 (1994) 10444-10450
40. Prochiantz A. Protein and peptide transduction, twenty years later a happy birthday. Adv. Drug. Deliv. Rev. 60 (2007) 448-451 10.1016/j.addr.2007.08.040
41. Chang H.C., Samaniego F., Nair B.C., Buonaguro L., and Ensoli B. HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11 (1997) 1421-1431
42. Tyagi M., Rusnati M., Presta M., and Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276 (2001) 3254-3261
43. Rusnati M., Coltrini D., Oreste P., Zoppetti G., Albini A., Noonan D., d'Adda di Fagagna F., Giacca M., and Presta M. Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size. J. Biol. Chem. 272 (1997) 11313-11320
44. Liu Y., Jones M., Hingtgen C.M., Bu G., Laribee N., Tanzi R.E., Moir R.D., Nath A., and He J.J. Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat. Med. 6 (2000) 1380-1387
45. Console S., Marty C., Garcia-Echeverria C., Schwendener R., and 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. J. Biol. Chem. 278 (2003) 35109-35114
46. Pellegrini L. Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr. Opin. Struct. Biol. 11 (2001) 629-634
47. Wu R.F., Gu Y., Xu Y.C., Mitola S., Bussolino F., and Terada L.S. Human immunodeficiency virus type 1 Tat regulates endothelial cell actin cytoskeletal dynamics through PAK1 activation and oxidant production. J. Virol. 78 (2004) 779-789
48. Mitola S., Sozzani S., Luini W., Primo L., Borsatti A., Weich H., and Bussolino F. Tat-human immunodeficiency virus-1 induces human monocyte chemotaxis by activation of vascular endothelial growth factor receptor-1. Blood 90 (1997) 1365-1372
49. Rubio Demirovic A., Canadi J., Weiglhofer W., Scheidegger P., Jaussi R., and Kurt B.H. HIV TAT basic peptide is not a high-affinity ligand for VEGF receptor 2. Biol. Chem. 384 (2003) 1435-1441
50. Fotin-Mleczek M., Welte S., Mader O., Duchardt F., Fischer R., Hufnagel H., Scheurich P., and Brock R. Cationic cell-penetrating peptides interfere with TNF signalling by induction of TNF receptor internalization. J. Cell Sci. 118 (2005) 3339-3351
51. Jones L.R., Goun E.A., Shinde R., Rothbard J.B., Contag C.H., and Wender P.A. Releasable luciferin-transporter conjugates: tools for the real-time analysis of cellular uptake and release. J. Am. Chem. Soc. 128 (2006) 6526-6527
52. Wender P.A., Goun E.A., Jones L.R., Pillow T.H., Rothbard J.B., Shinde R., and Contag C.H. Real-time analysis of uptake and bioactivatable cleavage of luciferin-transporter conjugates in transgenic reporter mice. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 10340-10345
53. + leukaemia cells. Biochem. J. 403 (2007) 335-342
54. Duchardt F., Fotin-Mleczek M., Schwarz H., Fischer R., and Brock R. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8 (2007) 848-866
55. Al-Taei S., Penning N.A., Simpson J.C., Futaki S., Takeuchi T., Nakase I., and Jones A.T. Intracellular traffic and fate of protein transduction domains HIV-1 TAT peptide and octaarginine. Implications for their utilization as drug delivery vectors. Bioconjug. Chem. 17 (2006) 90-100
56. Takeuchi T., Kosuge M., Tadokoro A., Sugiura Y., Nishi M., Kawata M., Sakai N., Matile S., and Futaki S. Direct and rapid cytosolic delivery using cell-penetrating peptides mediated by pyrenebutyrate. ACS Chem. Biol. 1 (2006) 299-303
57. Perret F., Nishihara M., Takeuchi T., Futaki S., Lazar A.N., Coleman A.W., Sakai N., and Matile S. Anionic fullerenes, calixarenes, coronenes, and pyrenes as activators of oligo/polyarginines in model membranes and live cells. J. Am. Chem. Soc. 127 (2005) 1114-1115
58. Nishihara M., Perret F., Takeuchi T., Futaki S., Lazar A.N., Coleman A.W., Sakai N., and Matile S. Arginine magic with new counterions up the sleeve. Org. Biomol. Chem. 3 (2005) 1659-1669
59. Sakai N., and Matile S. Anion-mediated transfer of polyarginine across liquid and bilayer membranes. J. Am. Chem. Soc. 125 (2003) 14348-14356
60. 125I-labeled Fab fragment in rats. Bioconjug. Chem. 17 (2006) 597-602
61. Umezawa N., Gelman M.A., Haigis M.C., Raines R.T., and Gellman S.H. Translocation of a beta-peptide across cell membranes. J. Am. Chem. Soc. 124 (2002) 368-369
62. Potocky T.B., Menon A.K., and Gellman S.H. Effects of conformational stability and geometry of guanidinium display on cell entry by beta-peptides. J. Am. Chem. Soc. 127 (2005) 3686-3687
63. Potocky T.B., Menon A.K., and Gellman S.H. Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells. J. Biol. Chem. 278 (2003) 50188-50194
64. Potocky T.B., Silvius J., Menon A.K., and Gellman S.H. HeLa cell entry by guanidinium-rich beta-peptides: importance of specific cation-cell surface interactions. Chembiochem 8 (2007) 917-926
65. Seebach D., Namoto K., Mahajan Y.R., Bindschadler P., Sustmann R., Kirsch M., Ryder N.S., Weiss M., Sauer M., Roth C., Werner S., Beer H.D., Munding C., Walde P., and Voser M. Chemical and biological investigations of beta-oligoarginines. Chem. Biodivers. 1 (2004) 65-97
66. Rueping M., Mahajan Y., Sauer M., and Seebach D. Cellular uptake studies with beta-peptides. Chembiochem 3 (2002) 257-259
67. Wender P.A., Rothbard J.B., Jessop T.C., Kreider E.L., and Wylie B.L. Oligocarbamate molecular transporters: design, synthesis, and biological evaluation of a new class of transporters for drug delivery. J. Am. Chem. Soc. 124 (2002) 13382-13383
68. Wender P.A., Mitchell D.J., Pattabiraman K., Pelkey E.T., Steinman L., and Rothbard J.B. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13003-13008
69. Futaki S., Nakase I., Suzuki T., Youjun Z., and Sugiura Y. Translocation of branched-chain arginine peptides through cell membranes: flexibility in the spatial disposition of positive charges in membrane-permeable peptides. Biochemistry 41 (2002) 7925-7930
70. Chung H.H., Harms G., Seong C.M., Choi B.H., Min C., Taulane J.P., and Goodman M. Dendritic oligoguanidines as intracellular translocators. Biopolymers 76 (2004) 83-96
71. Wender P.A., Kreider E., Pelkey E.T., Rothbard J., and Vandeusen C.L. Dendrimeric molecular transporters: synthesis and evaluation of tunable polyguanidino dendrimers that facilitate cellular uptake. Org. Lett. 7 (2005) 4815-4818
72. Huang K., Voss B., Kumar D., Hamm H.E., and Harth E. Dendritic molecular transporters provide control of delivery to intracellular compartments. Bioconjug. Chem. 18 (2007) 403-409
73. Luedtke N.W., Carmichael P., and Tor Y. Cellular uptake of aminoglycosides, guanidinoglycosides, and poly-arginine. J. Am. Chem. Soc. 125 (2003) 12374-12375
74. Elson-Schwab L., Garner O.B., Schuksz M., Crawford B.E., Esko J.D., and Y. Tor. Guanidinylated neomycin delivers large, bioactive cargo into cells through a heparan sulfate-dependent pathway. J. Biol. Chem. 282 (2007) 13585-13591
75. Maiti K.K., Jeon O.Y., Lee W.S., Kim D.C., Kim K.T., Takeuchi T., Futaki S., and Chung S.K. Design, synthesis, and membrane-translocation studies of inositol-based transporters, Angew. Chem. Int. Ed. Engl. 45 (2006) 2907-2912
76. Maiti K.K., Lee W.S., Takeuchi T., Watkins C., Fretz M., Kim D.C., Futaki S., Jones A., Kim K.T., and Chung S.K. Guanidine-containing molecular transporters: sorbitol-based transporters show high intracellular selectivity toward mitochondria. Angew. Chem., Int. Ed. Engl. 46 (2007) 5880-5884
77. Okuyama M., Laman H., Kingsbury S.R., Visintin C., Leo E., Eward K.L., Stoeber K., Boshoff C., Williams G.H., and Selwood D.L. Small-molecule mimics of an alpha-helix for efficient transport of proteins into cells. Nat. Methods 4 (2007) 153-159
78. Pujals S., Fernandez-Carneado J., Kogan M.J., Martinez J., Cavelier F., and Giralt E. Replacement of a proline with silaproline causes a 20-fold increase in the cellular uptake of a Pro-rich peptide. J. Am. Chem. Soc. 128 (2006) 8479-8483
79. Farrera-Sinfreu J., Giralt E., Castel S., Albericio F., and Royo M. Cell-penetrating cis-gamma-amino-l-proline-derived peptides. J. Am. Chem. Soc. 127 (2005) 9459-9468
80. Pujals S., Sabido E., Tarrago T., and Giralt E. All-D proline-rich cell-penetrating peptides: a preliminary in vivo internalization study. Biochem. Soc. Trans. 35 (2007) 794-796
81. Fillon Y.A., Anderson J.P., and Chmielewski J. Cell penetrating agents based on a polyproline helix scaffold. J. Am. Chem. Soc. 127 (2005) 11798-11803
82. Deglane G., Abes S., Michel T., Prevot P., Vives E., Debart F., Barvik I., Lebleu B., and Vasseur J.J. Impact of the guanidinium group on hybridization and cellular uptake of cationic oligonucleotides. Chembiochem 7 (2006) 684-692
83. Dragulescu-Andrasi A., Rapireddy S., He G., Bhattacharya B., Hyldig-Nielsen J.J., Zon G., and Ly D.H. Cell-permeable peptide nucleic acid designed to bind to the 5′ -untranslated region of E-cadherin transcript induces potent and sequence-specific antisense effects. J. Am. Chem. Soc. 128 (2006) 16104-16112
84. Zhou P., Wang M., Du L., Fisher G.W., Waggoner A., and Ly D.H. Novel binding and efficient cellular uptake of Guanidine-Based Peptide Nucleic Acids (GPNA). J. Am. Chem. Soc. 125 (2003) 6878-6879
85. Fuchs S.M., and Raines R.T. Arginine grafting to endow cell permeability. ACS Chem. Biol. 2 (2007) 167-170
86. Litovchick A., Lapidot A., Eisenstein M., Kalinkovich A., and Borkow G. Neomycin B-arginine conjugate, a novel HIV-1 Tat antagonist: synthesis and anti-HIV activities. Biochemistry 40 (2001) 15612-15623
87. Sanderson R.D., Yang Y., Suva L.J., and Kelly T. Heparan sulfate proteoglycans and heparanase-partners in osteolytic tumor growth and metastasis. Matrix Biol. 23 (2004) 341-352
88. Sasisekharan R., Shriver Z., Venkataraman G., and Narayanasami U. Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer 2 (2002) 521-528
89. Fernandez-Carneado J., Van Gool M., Martos V., Castel S., Prados P., de Mendoza J., and Giralt E. Highly efficient, nonpeptidic oligoguanidinium vectors that selectively internalize into mitochondria. J. Am. Chem. Soc. 127 (2005) 869-874