Molecular partners for interaction and cell internalization of cell-penetrating peptides: How identical are they?

Nanomedicine

Volumn 7, Issue 1, 2012, Pages 133-143

  Walrant, Astrid ^a,b,c   Bechara, Chérine ^a,b,c   Alves, Isabel D ^b   Sagan, Sandrine ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c Centre National de la Recherche Scientifique   (France)

Author keywords

actin; cell penetrating peptide; delivery; glycosaminoglycans; internalization; membrane domain; pinocytosis; translocation

Indexed keywords

ARGININE DERIVATIVE; CARBOHYDRATE; CELL PENETRATING PEPTIDE; GLYCOSAMINOGLYCAN; GUANIDINE; LIPID; OLIGOARGININE; PENETRATIN; SULFATE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BINDING AFFINITY; CELL INTERACTION; CELL SURFACE; CELL TYPE; CONCENTRATION (PARAMETERS); HYDROGEN BOND; LIPID MEMBRANE; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW;

BINDING SITES; CARBOHYDRATES; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; ENDOCYTOSIS; GLYCOSAMINOGLYCANS; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; PEPTIDES; PINOCYTOSIS;

EID: 84555202707     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.165     Document Type: Review

References (95)

1. Berry CC. Intracellular delivery of nanoparticles via the HIV-1 tat peptide. Nanomedicine 3(3), 357-365 (2008). (Pubitemid 351827312)
2. Juliano RL, Alam R, Dixit V, Kang HM. Cell-targeting and cell-penetrating peptides for delivery of therapeutic and imaging agents. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1(3), 324-335 (2009).
3. Moulton HM, Fletcher S, Neuman BW et al. Cell-penetrating peptide-morpholino conjugates alter pre-mRNA splicing of DMD (Duchenne muscular dystrophy) and inhibit murine coronavirus replication in vivo. Biochem. Soc. Trans. 35(Pt 4), 826-828 (2007). (Pubitemid 47310377)
4. Dietz GP. Cell-penetrating peptide technology to deliver chaperones and associated factors in diseases and basic research. Curr. Pharm. Biotechnol. 11(2), 167-174 (2010).
5. Said Hassane F, Saleh AF, Abes R, Gait MJ, Lebleu B. Cell penetrating peptides: overview and applications to the delivery of oligonucleotides. Cell. Mol. Life Sci. 67(5), 715-726 (2010).
6. Ezzat K, Andaloussi SE, Zaghloul EM et al. PepFect 14, a novel cell-penetrating peptide for oligonucleotide delivery in solution and as solid formulation. Nucleic Acids Res. 39(12), 5284-5298 (2011).
7. Boisguerin P, Redt-Clouet C, Franck-Miclo A et al. Systemic delivery of BH4 anti-apoptotic peptide using CPPs prevents cardiac ischemia-reperfusion injuries in vivo. J. Control. Release 156(2), 146-153 (2011).
8. Matsushita M, Tomizawa K, Moriwaki A, Li ST, Terada H, Matsui H. A high-effciency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. J. Neurosci. 21(16), 6000-6007 (2001). (Pubitemid 32737733)
9. Faruque OM, Le-Nguyen D, Lajoix AD et al. Cell-permeable peptide-based disruption of endogenous PKA-AKAP complexes: a tool for studying the molecular roles of AKAP-mediated PKA subcellular anchoring. Am. J. Physiol. Cell Physiol. 296(2), C306-C316 (2009).
10. Lee CY, Li JF, Liou JS, Charng YC, Huang YW, Lee HJ. A gene delivery system for human cells mediated by both a cell-penetrating peptide and a piggyBac transposase. Biomaterials 32(26), 6264-6276 (2011).
11. Todorova R. Comparative ana lysis of the methods of drug and protein delivery for the treatment of cancer, genetic diseases and diagnostics. Drug Deliv. doi:10.3109/1071754 4.2011.600783 (2011) (Epub ahead of print).
12. Hai-Tao Z, Hui-Cheng L, Zheng-Wu L, Chang-Hong G. A tumor-penetrating peptide modifcation enhances the antitumor activity of endostatin in vivo. Anticancer Drugs 22(5), 409-415 (2011).
13. Watkins CL, Sayers EJ, Allender C et al. Co-operative membrane disruption between cell-penetrating peptide and cargo: implications for the therapeutic use of the Bcl-2 converter peptide D-NuBCP-9-r8. Mol. Ther. doi:10.1038/mt.2011. 175 (2011) (Epub ahead of print).
14. El Andaloussi S, Said Hassane F, Boisguerin P, Sillard R, Langel U, Lebleu B. Cell-penetrating peptides-based strategies for the delivery of splice redirecting antisense oligonucleotides. Methods Mol. Biol. 764, 75-89 (2011).
15. Grdisa M. The delivery of biologically active (therapeutic) peptides and proteins into cells. Curr. Med. Chem. 18(9), 1373-1379 (2011).
16. Kurzawa L, Pellerano M, Coppolani JB, Morris MC. Fluorescent peptide biosensor for probing the relative abundance of cyclin-dependent kinases in living cells. PLoS ONE 6(10), e26555 (2011).
17. Vukojevic V, Graslund A, Bakalkin G. Fluorescence imaging with single-molecule sensitivity and fuorescence correlation spectroscopy of cell-penetrating neuropeptides. Methods Mol. Biol. 789, 147-170 (2011).
18. Crombez L, Morris MC, Dufort S et al. Targeting cyclin B1 through peptide-based delivery of siRNA prevents tumour growth. Nucleic Acids Res. 37(14), 4559-4569 (2009).
19. Deshayes S, Konate K, Aldrian G, Crombez L, Heitz F, Divita G. Structural polymorphism of non-covalent peptide-based delivery systems: highway to cellular uptake. Biochim. Biophys. Acta 1798(12), 2304-2314 (2010).
20. Madani F, Peralvarez-Marin A, Graslund A. Liposome model systems to study the endosomal escape of cell-penetrating peptides: transport across phospholipid membranes induced by a proton gradient. J. Drug Deliv. 2011, 897592 (2011).
21. El-Sayed A, Futaki S, Harashima H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J. 11(1), 13-22 (2009).
22. 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. 60(4-5), 598-607 (2008). (Pubitemid 351215576)
23. Ziegler A. Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv. Drug Deliv. Rev. 60(4-5), 580-597 (2008). (Pubitemid 351215575)
24. Ziegler A, Seelig J. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters. Biophys. J. 86(1 Pt 1), 254-263 (2004). (Pubitemid 38067453)
25. 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 44(7), 2692-2702 (2005). (Pubitemid 40279574)
26. Ziegler A, Seelig J. Binding and clustering of glycosaminoglycans: a common property of mono-and multivalent cell-penetrating compounds. Biophys. J. 94(6), 2142-2149 (2008).
27. Ziegler A, Seelig J. Contributions of glycosaminoglycan binding and clustering to the biological uptake of the nonamphipathic cell-penetrating peptide WR9. Biochemistry 50(21), 4650-4664 (2011).
28. Ghibaudi E, Boscolo B, Inserra G et al. The interaction of the cell-penetrating peptide penetratin with heparin, heparansulfates and phospholipid vesicles investigated by ESR spectroscopy. J. Pept. Sci. 11(7), 401-409 (2005). (Pubitemid 40959940)
29. Rullo A, Qian J, Nitz M. Peptide-glycosaminoglycan cluster formation involving cell penetrating peptides. Biopolymers 95(10), 722-731 (2011).
30. Alves ID, Jiao CY, Aubry S et al. Cell biology meets biophysics to unveil the different mechanisms of penetratin internalization in cells. Biochim. Biophys. Acta 1798(12), 2231-2239 (2010).
31. Berlose JP, Convert O, Derossi D, Brunissen A, Chassaing G. Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments. Eur. J. Biochem. 242(2), 372-386 (1996). (Pubitemid 26414244)
32. Magzoub M, Kilk K, Eriksson LE, Langel U, Graslund A. Interaction and structure induction of cell-penetrating peptides in the presence of phospholipid vesicles. Biochim. Biophys. Acta 1512(1), 77-89 (2001). (Pubitemid 32378784)
33. Alves ID, Goasdoue N, Correia I et al. Membrane interaction and perturbation mechanisms induced by two cationic cell penetrating peptides with distinct charge distribution. Biochim. Biophys. Acta 1780(7-8), 948-959 (2008).
34. Eiriksdottir E, Konate K, Langel U, Divita G, Deshayes S. Secondary structure of cell-penetrating peptides controls membrane interaction and insertion. Biochim. Biophys. Acta 1798(6), 1119-1128 (2010).
35. Walrant A, Correia I, Jiao CY et al. Different membrane behaviour and cellular uptake of three basic arginine-rich peptides. Biochim. Biophys. Acta 1808(1), 382-393 (2011).
36. Takechi Y, Yoshii H, Tanaka M, Kawakami T, Aimoto S, Saito H. Physicochemical mechanism for the enhanced ability of lipid membrane penetration of polyarginine. Langmuir 27(11), 7099-7107 (2011).
37. Persson D, Thoren PE, Herner M, Lincoln P, Norden B. Application of a novel ana lysis to measure the binding of the membrane-translocating peptide penetratin to negatively charged liposomes. Biochemistry 42(2), 421-429 (2003). (Pubitemid 36105760)
38. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269(14), 10444-10450 (1994). (Pubitemid 24198241)
39. Maniti O, Alves I, Trugnan G, Ayala-Sanmartin J. Distinct behaviour of the homeodomain derived cell penetrating peptide penetratin in interaction with different phospholipids. PLoS ONE 5(12), e15819 (2010).
40. Magzoub M, Eriksson LE, Graslund A. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles: effects of surface charge and peptide concentration. Biochim. Biophys. Acta 1563(1-2), 53-63 (2002). (Pubitemid 34455043)
41. 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. J. Biol. Chem. 271(30), 18188-18193 (1996). (Pubitemid 26250811)
42. Ye J, Fox SA, Cudic M et al. Determination of penetratin secondary structure in live cells with Raman microscopy. J. Am. Chem. Soc. 132(3), 980-988 (2010).
43. Lattig-Tunnemann G, Prinz M, Hoffmann D et al. Backbone rigidity and static presentation of guanidinium groups increases cellular uptake of arginine-rich cell-penetrating peptides. Nat. Commun. 2, 453 (2011).
44. Salamon Z, Macleod HA, Tollin G. Coupled plasmon-waveguide resonators: a new spectroscopic tool for probing proteolipid flm structure and properties. Biophys. J. 73(5), 2791-2797 (1997). (Pubitemid 27471488)
45. Alves ID, Park CK, Hruby VJ. Plasmon resonance methods in GPCR signaling and other membrane events. Curr. Protein Pept. Sci. 6(4), 293-312 (2005). (Pubitemid 41052400)
46. 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. 84(3), 1796-1807 (2003). (Pubitemid 36322941)
47. Salamon Z, Tollin G. Graphical ana lysis of mass and anisotropy changes observed by plasmon-waveguide resonance spectroscopy can provide useful insights into membrane protein function. Biophys. J. 86(4), 2508-2516 (2004). (Pubitemid 38524437)
48. Alves ID, Correia I, Jiao CY et al. The interaction of cell-penetrating peptides with lipid model systems and subsequent lipid reorganization: thermodynamic and structural characterization. J. Pept. Sci. 15(3), 200-209 (2009).
49. Alves ID, Bechara C, Walrant A, Zaltsman Y, Jiao CY, Sagan S. Relationships between membrane binding, affnity and cell internalization effcacy of a cell-penetrating peptide: penetratin as a case study. PLoS ONE 6(9), e24096 (2011).
50. Drin G, Demene H, Temsamani J, Brasseur R. Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry 40(6), 1824-1834 (2001). (Pubitemid 32144055)
51. Christiaens B, Symoens S, Verheyden S et al. Tryptophan fuorescence study of the interaction of penetratin peptides with model membranes. Eur. J. Biochem. 269(12), 2918-2926 (2002). (Pubitemid 34754020)
52. Binder H, Lindblom G. Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes. Biophys. J. 85(2), 982-995 (2003). (Pubitemid 36909662)
53. Ziegler A, Blatter XL, Seelig A, Seelig J. Protein transduction domains of HIV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic ana lysis. Biochemistry 42(30), 9185-9194 (2003). (Pubitemid 36935428)
54. Tiriveedhi V, Butko P. A Fluorescence Spectroscopy study on the interactions of the TAT-PTD peptide with model lipid membranes. Biochemistry 46(12), 3888-3895 (2007). (Pubitemid 46493489)
55. Thoren PE, Persson D, Esbjorner EK, Goksor M, Lincoln P, Norden B. Membrane binding and translocation of cell-penetrating peptides. Biochemistry 43(12), 3471-3489 (2004). (Pubitemid 38391703)
56. Schwieger C, Blume A. Interaction of poly(L-arginine) with negatively charged DPPG membranes: calorimetric and monolayer studies. Biomacromolecules 10(8), 2152-2161 (2009).
57. Sakai N, Matile S. Anion-mediated transfer of polyarginine across liquid and bilayer membranes. J. Am. Chem. Soc. 125(47), 14348-14356 (2003). (Pubitemid 37452373)
58. 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. 126(31), 9506-9507 (2004). (Pubitemid 39031015)
59. Esbjorner EK, Lincoln P, Norden B. Counterion-mediated membrane penetration: cationic cell-penetrating peptides overcome Born energy barrier by ion-pairing with phospholipids. Biochim. Biophys. Acta 1768(6), 1550-1558 (2007). (Pubitemid 46782707)
60. Thoren PE, Persson D, Lincoln P, Norden B. Membrane destabilizing properties of cell-penetrating peptides. Biophys. Chem. 114(2-3), 169-179 (2005). (Pubitemid 40521515)
61. Joanne P, Galanth C, Goasdoue N et al. Lipid reorganization induced by membrane-active peptides probed using differential scanning calorimetry. Biochim. Biophys. Acta 1788(9), 1772-1781 (2009).
62. Baumgartner P, Geiger M, Zieseniss S et al. Phosphatidylethanolamine critically supports internalization of cell-penetrating protein C inhibitor. J. Cell. Biol. 179(4), 793-804 (2007). (Pubitemid 350146262)
63. Jones AT. Gateways and tools for drug delivery: endocytic pathways and the cellular dynamics of cell penetrating peptides. Int. J. Pharm. 354(1-2), 34-38 (2008).
64. Amand HL, Fant K, Norden B, Esbjorner EK. Stimulated endocytosis in penetratin uptake: effect of arginine and lysine. Biochem. Biophys. Res. Commun. 371(4), 621-625 (2008).
65. Wadia JS, Dowdy SF. Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Adv. Drug Deliv. Rev. 57(4), 579-596 (2005). (Pubitemid 40255562)
66. Richard JP, Melikov K, Vives E et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278(1), 585-590 (2003). (Pubitemid 36043612)
67. Ter-Avetisyan G, Tunnemann G, Nowak D et al. Cell entry of arginine-rich peptides is independent of endocytosis. J. Biol. Chem. 284(6), 3370-3378 (2009).
68. Joliot AH, Triller A, Volovitch M, Pernelle C, Prochiantz A. Alpha-2,8-polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide. New Biol. 3(11), 1121-1134 (1991).
69. Yang H, Liu S, Cai H et al. Chondroitin sulfate as a molecular portal that preferentially mediates the apoptotic killing of tumor cells by penetratin-directed mitochondria-disrupting peptides. J. Biol. Chem. 285(33), 25666-25676 (2010).
70. Melikov K, Chernomordik LV. Arginine-rich cell penetrating peptides: from endosomal uptake to nuclear delivery. Cell. Mol. Life Sci. 62(23), 2739-2749 (2005). (Pubitemid 41779944)
71. Console S, Marty C, Garcia-Echeverria 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. J. Biol. Chem. 278(37), 35109-35114 (2003). (Pubitemid 37102274)
72. Fuchs SM, Raines RT. Pathway for polyarginine entry into mammalian cells. Biochemistry 43(9), 2438-2444 (2004). (Pubitemid 38327839)
73. Jiao CY, Delaroche D, Burlina F, Alves ID, Chassaing G, Sagan S. Translocation and endocytosis for cell-penetrating peptide internalization. J. Biol. Chem. 284(49), 33957-33965 (2009).
74. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J. Studies on the internalization mechanism of cationic cell-penetrating peptides. J. Biol. Chem. 278(33), 31192-31201 (2003). (Pubitemid 36994635)
75. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffc 8(7), 848-866 (2007). (Pubitemid 46971632)
76. Saar K, Lindgren M, Hansen M et al. Cell-penetrating peptides: a comparative membrane toxicity study. Anal. Biochem. 345(1), 55-65 (2005). (Pubitemid 41558194)
77. El-Andaloussi S, Jarver P, Johansson HJ, Langel U. Cargo-dependent cytotoxicity and delivery effcacy of cell-penetrating peptides: a comparative study. Biochem. J. 407(2), 285-292 (2007). (Pubitemid 47556993)
78. 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. 19(3), 656-664 (2008). (Pubitemid 351431397)
79. Aubry S, Burlina F, Dupont E et al. Cell-surface thiols affect cell entry of disulfde-conjugated peptides. FASEB J. 23(9), 2956-2967 (2009).
80. 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. 420(2), 179-189 (2009).
81. Magzoub M, Pramanik A, Graslund A. Modeling the endosomal escape of cell-penetrating peptides: transmembrane pH gradient driven translocation across phospholipid bilayers. Biochemistry 44(45), 14890-14897 (2005). (Pubitemid 41612268)
82. Gump JM, June RK, Dowdy SF. Revised role of glycosaminoglycans in TAT protein transduction domain-mediated cellular transduction. J. Biol. Chem. 285(2), 1500-1507 (2009).
83. Puckett CA, Barton JK. Fluorescein redirects a ruthenium-octaarginine conjugate to the nucleus. J. Am. Chem. Soc. 131(25), 8738-8739 (2009).
84. Puckett CA, Barton JK. Targeting a ruthenium complex to the nucleus with short peptides. Bioorg. Med. Chem. 18(10), 3564-3569 (2010).
85. Saalik P, Elmquist A, Hansen M et al. Protein cargo delivery properties of cell-penetrating peptides. A comparative study. Bioconjug. Chem. 15(6), 1246-1253 (2004). (Pubitemid 39552013)
86. 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. 20(11), 1775-1784 (2006). (Pubitemid 44933791)
87. Aussedat B, Dupont E, Sagan S et al. Modifcations in the chemical structure of Trojan carriers: impact on cargo delivery. Chem. Commun. (12), 1398-1400 (2008). (Pubitemid 351367591)
88. 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. 269(2), 494-501 (2002). (Pubitemid 34128006)
89. Delaroche D, Cantrelle FX, Subra F et al. Cell-penetrating peptides with intracellular actin-remodeling activity in malignant fbroblasts. J. Biol. Chem. 285(10), 7712-7721 (2010).
90. 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 108(41), 16883-16888 (2011).
91. Raagel H, Saalik P, Pooga M. Peptide-mediated protein delivery-which pathways are penetrable? Biochim. Biophys. Acta 1798(12), 2240-2248 (2010).
92. Herce HD, Garcia AE. Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc. Natl Acad. Sci. USA 104(52), 20805-20810 (2007).
93. Herce HD, Garcia AE, Litt J et al. Arginine-rich peptides destabilize the plasma membrane, consistent with a pore formation translocation mechanism of cell-penetrating peptides. Biophys. J. 97(7), 1917-1925 (2009).
94. Palm-Apergi C, Lorents A, Padari K, Pooga M, Hallbrink M. The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake. FASEB J. 23(1), 214-223 (2009).
95. Rothbard JB, Jessop TC, Wender PA. Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells. Adv. Drug Deliv. Rev. 57(4), 495-504 (2005). (Pubitemid 40255557)