Arginine-rich peptides: Methods of translocation through biological membranes

Current Pharmaceutical Design

Volumn 19, Issue 16, 2013, Pages 2863-2868

  Futaki, Shiroh ^a   Hirose, Hisaaki ^a   Nakase, Ikuhiko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Arginine; Cell penetrating peptide; Counterion; Direct translocation; Macropinocytosis; Membrane curvature; Membrane potential; Membrane associated proteoglycan

Indexed keywords

ARGININE; CELL PENETRATING PEPTIDE; LYSINE; POLYPEPTIDE ANTIBIOTIC AGENT;

AMINO ACID SEQUENCE; CAVEOLA; CELL MEMBRANE; CELL SURFACE; CHANNEL GATING; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CYTOTOXICITY; ENDOCYTOSIS; HELA CELL; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; INTERNALIZATION; INTRACELLULAR SIGNALING; LIPID BILAYER; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; STATIC ELECTRICITY;

ARGININE; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; DRUG DELIVERY SYSTEMS; HUMANS; PROTEIN TRANSPORT;

EID: 84878668366     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319160003     Document Type: Review

References (57)

1. Futaki S, Ed. Special theme issue on membrane permeable peptide vectors: chemistry and functional design for the therapeutic applications. Adv Drug Deliv Rev 2008; 60: 447-614.
2. El-Sayed A, Futaki S, Harashima H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J 2009; 11: 13-22.
3. Langel U, Ed. Handbook of cell-penetrating peptides. 2nd ed. London: CRC Press 2006.
4. Raghuraman H, Chattopadhyay A. Melittin: a membrane-active peptide with diverse functions. Biosci Rep 2007; 27:189-223.
5. Frankel AD, Pabo CO, Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55: 1189-93.
6. Green M, Loewenstein PM, Autonomous functional domains of chemically synthesized human immunodeficiency virus tat transactivator protein. Cell 1988; 55: 1179-88.
7. Perez F, Joliot A, Bloch-Gallego E, Zahraoui A, Triller A, Prochiantz A. Antennapedia homeobox as a signal for the cellular internalization and nuclear addressing of a small exogenous peptide. J Cell Sci 1992; 102: 717-22.
8. Joliot A, Prochiantz A. Transduction peptides: from technology to physiology. Nat Cell Biol 2004; 6: 189-96.
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. Derossi D, Joliot A. H, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes, J Biol Chem 1994; 269: 10444-50.
11. Rothbard JB, Garlington S, Lin Q, et al. Conjugation of arginine oligomers to cyclosporin A facilitates topical delivery and inhibition of inflammation. Nat Med 2000; 6: 1253-7.
12. Futaki S, Suzuki T, Ohashi W, et al. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 2001; 276: 5836-40.
13. Futaki S, Goto S, Suzuki T, Nakase I, Sugiura Y. Structural variety of membrane permeable peptides. Curr Protein Pept Sci 2003; 4: 87-96.
14. Nakase I, Hirose H, Tanaka G, et al. Cell-surface accumulation of flock house virus-derived peptide leads to efficient internalization via macropinocytosis. Mol Ther 2009; 17: 1868-76.
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. Richard JP, Melikov K, Vives E, et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003; 278: 585-90.
17. 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: 15300-6.
18. Wadia, JS, Stan, RV and Dowdy, SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10: 310-315.
19. Nakase I, Niwa M, Takeuchi T, et al. Cellular uptake of argininerich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther 2004; 10:1011-22.
20. Nakase I, Tadokoro A, Kawabata N, et al. Interaction of argininerich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 2007; 46: 492-501.
21. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003; 422: 37-44.
22. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R. A comprehensive model for the cellular uptake of cationic cellpenetrating peptides. Traffic 2007; 8: 848-66.
23. Jones AT, Sayers EJ. Cell entry of cell penetrating peptides: tales wagging dogs. J Control Release 2012; (in press).
24. Nakase I, Takeuchi T, Tanaka G, Futaki S. Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides. Adv Drug Deliv Rev 2008; 60: 598-607.
25. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim Biophys Acta 1998; 1376: 391-400.
26. Kosuge M, Takeuchi T, Nakase I, Jones AT, Futaki S. Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans. Bioconjug Chem 2008; 19: 656-64.
27. Katayama S, Hirose H, Takayama K, Nakase I, Futaki S. Acylation of octaarginine: Implication to the use of intracellular delivery vectors. J Control Release 2011; 149: 29-35.
28. Takayama K, Nakase I, Michiue H, et al. Enhanced intracellular delivery using arginine-rich peptides by the addition of penetration accelerating sequences (Pas). J Control Release 2009; 138: 128-33.
29. Hirose H, Takeuchi T, Osakada H, et al. Transient focal membrane deformation induced by arginine-rich peptides leads to their direct penetration into cells. Mol Ther 2012; 20: 984-93.
30. Verdurmen WP, Thanos M, Ruttekolk IR, Gulbins E, Brock R. Cationic cell-penetrating peptides induce ceramide formation via acid sphingomyelinase: implications for uptake. J Control Release 2010; 147: 171-9.
31. Lamaziere A, Wolf C, Lambert O, Chassaing, G, Trugnan G, Ayala-Sanmartin J. The homeodomain derived peptide Penetrati induces curvature of fluid membrane domains. PLoS One 2008; 3: e1938.
32. Afonin S, Frey A, Bayerl S, et al. The cell-penetrating peptide TAT(48-60) induces a non-lamellar phase in DMPC membranes. Chemphyschem 2006; 7: 2134-42.
33. Mishra A, Gordon VD, Yang L, Coridan R, Wong, GC. HIV TAT forms pores in membranes by inducing saddle-splay curvature: potential role of bidentate hydrogen bonding. Angew Chem Int Ed Engl 2008; 47: 2986-9.
34. Mishra A, Lai GH, Schmidt NW, et al. Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions. Proc Natl Acad Sci USA 2011; 108: 16883-8.
35. Sakamoto K, Takino Y, Ogasawara K, inventor; Methods for controlling membrane permeability of a membrane permeable substance and screening methods for a membrane permeable substance. United State Patent 2005/0118204, 2005 Jun 2.
36. Fretz M, Jin J, Conibere R, et al. 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: 247-54.
37. Jones AT. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 2007; 11: 670-84.
38. Suzuki T, Futaki S, Niwa M, Tanaka S, Ueda K, Sugiura Y. Possible existence of common internalization mechanisms among arginine-rich peptides. J Biol Chem 2002; 277: 2437-43.
39. Watkins CL, Schmaljohann D, Futaki S, Jones AT. Low concentration thresholds of plasma membranes for rapid energy-independent translocation of a cell-penetrating peptide. Biochem J 2009; 420: 179-89.
40. Mercer J, Helenius A. Virus entry by macropinocytosis. Nat Cell Biol 2009; 11: 510-20.
41. Fender P, Hall K, Schoehn G, Blair GE. Impact of human adenovirus type 3 dodecahedron on host cells and its potential role in viral infection. J Virol 2012; 86(9): 5380-5.
42. Villegas-Mendez A, Garin MI, Pineda-Molina E, et al. In vivo delivery of antigens by adenovirus dodecahedron induces cellular and humoral immune responses to elicit antitumor immunity. Mol Ther 2010; 18(5):1046-53.
43. Fretz MM, Penning NA, Al-Taei S, et al. Temperature-, concentration-and cholesterol-dependent translocation of L-and D-octaarginine across the plasma and nuclear membrane of CD34+ leukaemia cells. Biochem J 2007; 403: 335-42.
44. Walrant A, Vogel A, Correia I, et al. Membrane interactions of two arginine-rich peptides with different cell internalization capacities. Biochim Biophys Acta 2012; 1818: 1755-63.
45. Lamazière A, Maniti O, Wolf C, et al. Lipid domain separation, bilayer thickening and pearling induced by the cell penetrating peptide penetratin. Biochim Biophys Acta 2010; 1798: 2223-30.
46. Takayama K, Hirose H, Tanaka G, et al. Effect of the attachment of a penetration accelerating sequence and the influence of hydrophobicity on octaarginine-mediated intracellular delivery. Mol Pharm 2012; 9: 1222-30.
47. Zhang X, Jin Y, Plummer MR, Pooyan S, Gunaseelan S, Sinko PJ. Endocytosis and membrane potential are required for HeLa cell uptake of R.I.-CKTat9, a retro-inverso Tat cell penetrating peptide. Mol Pharm 2009; 6: 836-48.
48. 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.
49. 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: 114-22.
50. Sakai N, Matile S. Anion-mediated transfer of polyarginine across liquid and bilayer membranes. J Am Chem Soc 2003; 125: 14348-56.
51. Perret F, Nishihara M, Takeuchi T, et al. Anionic fullerenes, calixarenes, coronenes, and pyrenes as activators of oligo/polyarginines in model membranes and live cells. J Am Chem Soc 2005; 127: 1114-5.
52. Nishihara M, Perret F, Takeuchi T, et al. Arginine magic with new counterions up the sleeve. Org Biomol Chem 2005; 3: 1659-69.
53. Takeuchi T, Kosuge M, Tadokoro A, et al. Direct and rapid cytosolic delivery using cell-penetrating peptides mediated by pyrenebutyrate, ACS Chem Biol 2006; 1: 299-303.
54. Inomata K, Ohno A, Tochio H, et al. High-resolution multidimensional NMR spectroscopy of proteins in human cells. Nature 2009; 458: 106-9.
55. Kamei N, Morishita M, Eda Y, Ida N, Nishio R, Takayama K. Usefulness of cell-penetrating peptides to improve intestinal insulin absorption. J Control Release 2008; 132: 21-5.
56. Sarko D, Beijer B, Garcia Boy R, et al. The pharmacokinetics of cell-penetrating peptides. Mol Pharm 2010; 7: 2224-31.
57. Nakase I, Konishi Y, Ueda M, Saji H, Futaki S. Accumulation of arginine-rich cell-penetrating peptides in tumors and the potential for anticancer drug delivery in vivo. J Control Release 2012; 159: 181-8.