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Review

Cell-penetrating peptides for drug delivery across membrane barriers

, MSc PhD & , MPharm PhD
Pages 105-117 | Published online: 21 Dec 2007

Bibliography

  • Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988;55(6):1189-93
  • Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 1988;55(6):1179-88
  • Joliot A, Pernelle C, Deagostinibazin H, Prochiantz A. Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci USA 1991;88(5):1864-8
  • 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(25):16010-17
  • Derossi D, Joliot AH, Chassaing G, Prochiantz A. The 3rd helix of the Antennapedia homeodomain translocates through biological-membranes. J Biol Chem 1994;269(14):10444-50
  • Fawell S, Seery J, Daikh Y, et al. Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 1994;91(2):664-8
  • Zorko M, Langel U. Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 2005;57(4):529-45
  • Snyder EL, Dowdy SF. Cell penetrating peptides in drug delivery. Pharm Res 2004;21(3):389-93
  • Richard JP, Melikov K, Vives E, et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003;278(1):585-90
  • Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science 1999;285(5433):1569-72
  • 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(8):5836-40
  • Pooga M, Hallbrink M, Zorko M, Langel U. Cell penetration by transportan. FASEB J 1998;12(1):67-77
  • Morris MC, Vidal P, Chaloin L, et al. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res 1997;25(14):2730-6
  • Morris MC, Depollier J, Mery J, et al. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 2001;19(12):1173-6
  • Lindgren M, Rosenthal-Aizman K, Saar K, et al. Overcoming methotrexate resistance in breast cancer tumour cells by the use of a new cell-penetrating peptide. Biochem Pharmacol 2006;71(4):416-25
  • Patel LN, Zaro JL, Shen WC. Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives. Pharm Res 2007;24(11):1977-92
  • Jones AT. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 2007;11(4):670-84
  • Pujals S, Fernandez-Carneado J, Lopez-Iglesias C, et al. Mechanistic aspects of CPP-mediated intracellular drug delivery: relevance of CPP self-assembly. Biochim Biophys Acta 2006;1758(3):264-79
  • Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 Tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 2001;276(5):3254-61
  • Nakase I, Tadokoro A, Kawabata N, et al. Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 2007;46(2):492-501
  • Foerg C, Ziegler U, Fernandez-Carneado J, et al. Differentiation restricted endocytosis of cell penetrating peptides in MDCK cells corresponds with activities of Rho-GTPases. Pharm Res 2007;24(4):628-42
  • Lundberg M, Johansson M. Positively charged DNA-binding proteins cause apparent cell membrane translocation. Biochem Biophys Res Commun 2002;291(2):367-71
  • Richard JP, Melikov K, Brooks H, et al. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J Biol Chem 2005;280(15):15300-6
  • Nakase I, Niwa M, Takeuchi T, et al. Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther 2004;10(6):1011-22
  • Shiraishi T, Nielsen PE. Photochemically enhanced cellular delivery of cell penetrating peptide-PNA conjugates. FEBS Lett 2006;580(5):1451-6
  • Wolf Y, Pritz S, Abes S, et al. Structural requirements for cellular uptake and antisense activity of peptide nucleic acids conjugated with various peptides. Biochemistry 2006;45(50):14944-54
  • Thoren PEG, Persson D, Karlsson M, Norden B. The Antennapedia peptide penetratin translocates across lipid bilayers – the first direct observation. FEBS Lett 2000;482(3):265-8
  • 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(47):13787-99
  • Henriques ST, Castanho MARB. Consequences of nonlytic membrane perturbation to the translocation of the cell penetrating peptide pep-1 in lipidic vesicles. Biochemistry 2004;43(30):9716-24
  • Zaro JL, Shen WC. Evidence that membrane transduction of oligoarginine does not require vesicle formation. Exp Cell Res 2005;307(1):164-73
  • Mano M, Henriques A, Paiva A, et al. Interaction of S413-PV cell penetrating peptide with model membranes: relevance to peptide translocation across biological membranes. J Pept Sci 2007;13(5):301-13
  • 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):114-22
  • Nishihara M, Perret F, Takeuchi T, et al. Arginine magic with new counterions up the sleeve. Org Biomol Chem 2005;3(9):1659-69
  • Rothbard JB, Jessop TC, Lewis RS, et al. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J Am Chem Soc 2004;126(31):9506-7
  • 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 2005;57(4):495-504
  • Duchardt F, Fotin-Mleczek M, Schwarz H, et al. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 2007;8(7):848-66
  • Fretz MM, Penning NA, Al Taei S, et al. Temperature-, concentration- and cholesterol-dependent translocation of L- and D-octa-arginine across the plasma and nuclear membrane of CD34+ leukaemia cells. Biochem J 2007;403(2):335-42
  • Palm C, Jayamanne M, Kjellander M, Hallbrink M. Peptide degradation is a critical determinant for cell-penetrating peptide uptake. Biochim Biophys Acta 2007;1768(7):1769-76
  • Trehin R, Nielsen HM, Jahnke HG, et al. Metabolic cleavage of cell-penetrating peptides in contact with epithelial models: human calcitonin (hCT)-derived peptides, Tat(47-57) and penetratin(43-58). Biochem J 2004;382(Part 3):945-56
  • Weller K, Lauber S, Lerch M, et al. Biophysical and biological studies of end-group-modified derivatives of Pep-1. Biochemistry 2005;44(48):15799-811
  • Aussedat B, Sagan S, Chassaing G, et al. Quantification of the efficiency of cargo delivery by peptidic and pseudo-peptidic Trojan carriers using MALDI-TOF mass spectrometry. Biochim Biophys Acta 2006;1758(3):375-83
  • Elmquist A, Langel U. In vitro uptake and stability study of pVEC and its all-D analog. Biol Chem 2003;384(3):387-93
  • Youngblood DS, Hatlevig SA, Hassinger JN, et al. Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug Chem 2007;18(1):50-60
  • Gammon ST, Villalobos VM, Prior JL, et al. Quantitative analysis of permeation peptide complexes labeled with Technetium-99m: chiral and sequence-specific effects on net cell uptake. Bioconjug Chem 2003;14(2):368-76
  • Rothbard JB, Kreider E, Vandeusen CL, et al. Arginine-rich molecular transporters for drug delivery: role of backbone spacing in cellular uptake. J Med Chem 2002;45(17):3612-18
  • Rennert R, Wespe C, Beck-Sickinger AG, Neundorf I. Developing novel hCT derived cell-penetrating peptides with improved metabolic stability. Biochim Biophys Acta 2006;1758(3):347-54
  • Turner JJ, Jones S, Fabani MM, et al. RNA targeting with peptide conjugates of oligonucleotides, siRNA and PNA. Blood Cells Mol Dis 2007;38(1):1-7
  • Turner JJ, Ivanova GD, Verbeure B, et al. Cell-penetrating peptide conjugates of peptide nucleic acids (PNA) as inhibitors of HIV-1 Tat-dependent trans-activation in cells. Nucleic Acids Res 2005;33(21):6837-49
  • Hallbrink M, Floren A, Elmquist A, et al. Cargo delivery kinetics of cell-penetrating peptides. Biochim Biophys Acta 2001;1515(2):101-9
  • Saar K, Lindgren M, Hansen M, et al. Cell-penetrating peptides: a comparative membrane toxicity study. Anal Biochem 2005;345(1):55-65
  • Myrberg H, Lindgren M, Langel U. Protein delivery by the cell-penetrating peptide YTA2. Bioconjug Chem 2007;18(1):170-4
  • Jones SW, Christison R, Bundell K, et al. Characterisation of cell-penetrating peptide-mediated peptide delivery. Br J Pharmacol 2005;145(8):1093-102
  • Orzaez M, Mondragon L, Marzo I, et al. Conjugation of a novel Apaf-1 inhibitor to peptide-based cell-membrane transporters: effective methods to improve inhibition of mitochondria-mediated apoptosis. Peptides 2007;28(5):958-68
  • Maiolo JR, Ferrer M, Ottinger EA. Effects of cargo molecules on the cellular uptake of arginine-rich cell-penetrating epeptides. Biochim Biophys Acta 2005;1712(2):161-72
  • Trehin R, Krauss U, Muff R, et al. Cellular internalization of human calcitonin derived peptides in MDCK monolayers: a comparative study with Tat(47-57) and penetratin(43-58). Pharm Res 2004;21(1):33-42
  • Cardozo AK, Buchillier V, Mathieu M, et al. Cell-permeable peptides induce dose- and length-dependent cytotoxic effects. Biochim Biophys Acta 2007;1768(9):2222-34
  • Morishita M, Kamei N, Ehara J, et al. A novel approach using functional peptides for efficient intestinal absorption of insulin. J Control Rel 2007;118(2):177-84
  • Wagstaff KM, Jans DA. Protein transduction: cell penetrating peptides and their therapeutic applications. Curr Med Chem 2006;13(12):1371-87
  • Gros E, Deshayes S, Morris MC, et al. A non-covalent peptide-based strategy for protein and peptide nucleic acid transduction. Biochim Biophys Acta 2006;1758(3):384-93
  • Barany-Wallje E, Gaur J, Lundberg P, et al. Differential membrane perturbation caused by the cell penetrating peptide Tp10 depending on attached cargo. FEBS Lett 2007;581(13):2389-93
  • Rousselle C, Smirnova M, Clair P, et al. The use of a new peptide vector-mediated strategy which bypasses brain P-gp for the transport of doxorubicin across the BBB. FASEB J 2000;14(8):A1480-A1480
  • Mazel M, Clair P, Rousselle C, et al. Doxorubicin-peptide conjugates overcome multidrug resistance. Anti-Cancer Drugs 2001;12(2):107-16
  • El Andaloussi S, Holm T, Langel U. Cell-penetrating peptides: mechanisms and applications. Curr Pharm Des 2005;11(28):3597-611
  • Gupta B, Levchenko TS, Torchilin VP. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev 2005;57(4):637-51
  • Smith MW, Gumbleton M. Endocytosis at the blood–brain barrier: from basic understanding to drug delivery strategies. J Drug Target 2006;14(4):191-214
  • Silhol M, Tyagi M, Giacca M, et al. 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(2):494-501
  • Beerens AM, Al Hadithy AF, Rots MG, Haisma HJ. Protein transduction domains and their utility in gene therapy. Curr Gene Ther 2003;3(5):486-94
  • Martin ME, Rice KG. Peptide-guided gene delivery. AAPS J 2007;9(1):E18-E29
  • Meade BR, Dowdy SF. Exogenous siRNA delivery using peptide transduction domains/cell penetrating peptides. Adv Drug Deliv Rev 2007;59(2-3):134-40
  • Muratovska A, Eccles MR. Conjugate for efficient delivery of short interfering RNA (siRNA) into mammalian cells. FEBS Lett 2004;558(1-3):63-8
  • Davidson TJ, Harel S, Arboleda VA, et al. Highly efficient small interfering RNA delivery to primary mammalian neurons induces MicroRNA-like effects before mRNA degradation. J Neurosci 2004;24(45):10040-6
  • Chiu YL, Ali A, Chu CY, et al. Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells. Chem Biol 2004;11(8):1165-75
  • Simeoni F, Morris MC, Heitz F, Divita G. Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res 2003;31(11):2717-24
  • Veldhoen S, Laufer SD, Trampe A, Restle T. Cellular delivery of small interfering RNA by a non-covalently attached cell-penetrating peptide: quantitative analysis of uptake and biological effect. Nucleic Acids Res 2006;34(22):6561-73
  • Lundberg P, El Andaloussi S, Sutlu T, et al. Delivery of short interfering RNA using endosomolytic cell-penetrating peptides. FASEB J 2007;21(11):2664-71
  • Pooga M, Soomets U, Hallbrink M, et al. Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat Biotechnol 1998;16(9):857-61
  • Abes S, Turner JJ, Ivanova GD, et al. Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide. Nucleic Acids Res 2007;35(13):4495-502
  • Resina S, Abes S, Turner JJ, et al. Lipoplex and peptide-based strategies for the delivery of steric-block oligonucleotides. Int J Pharm 2007;344(1-2):96-102
  • Bendifallah N, Rasmussen FW, Zachar V, et al. Evaluation of cell-penetrating peptides (CPPs) as vehicles for intracellular delivery of antisense peptide nucleic acid (PNA). Bioconjug Chem 2006;17(3):750-8
  • Kilk K, El Andaloussi S, Jarver P, et al. Evaluation of transportan 10 in PEI mediated plasmid delivery assay. J Control Rel 2005;103(2):511-23
  • Ignatovich IA, Dizhe EB, Pavlotskaya AV, et al. Complexes of plasmid DNA with basic domain 47-57 of the HIV-1 Tat protein are transferred to mammalian cells by endocytosis-mediated pathways. J Biol Chem 2003;278(43):42625-36
  • Eguchi A, Akuta T, Okuyama H, et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem 2001;276(28):26204-10
  • Liu ZH, Li MY, Cui DF, Fei J. Macro-branched cell-penetrating peptide design for gene delivery. J Control Rel 2005;102(3):699-710
  • Torchilin VP, Rammohan R, Weissig V, Levchenko TS. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc Natl Acad Sci USA 2001;98(15):8786-91
  • Zhang CL, Tang N, Liu XJ, et al. siRNA-containing liposomes modified with polyarginine effectively silence the targeted gene. J Control Rel 2006;112(2):229-39
  • Nakamura Y, Kogure K, Futaki S, Harashima H. Octaarginine-modified multifunctional envelope-type nano device for siRNA. J Control Rel 2007;119(3):360-7
  • Kleemann E, Neu M, Jekel N, et al. Nano-carriers for DNA delivery to the lung based upon a TAT-derived peptide covalently coupled to PEG-PEI. J Control Rel 2005;109(1-3):299-316
  • Sethuraman VA, Bae YH. TAT peptide-based micelle system for potential active targeting of anti-cancer agents to acidic solid tumors. J Control Rel 2007;118(2):216-24
  • Lewin M, Carlesso N, Tung CH, et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 2000;18(4):410-14
  • Lagerholm BC. Peptide-mediated intracellular delivery of quantum dots. Methods Mol Biol 2007;374:105-12
  • Torchilin VP. Tatp-mediated intracellular delivery of pharmaceutical nanocarriers. Biochem Soc Trans 2007;35(Part 4):816-20
  • Kale AA, Torchilin VP. Design, synthesis, and characterization of pH-sensitive PEG-PE conjugates for stimuli-sensitive pharmaceutical nanocarriers: the effect of substitutes at the hydrazone linkage on the pH stability of PEG-PE conjugates. Bioconjug Chem 2007;18(2):363-70
  • Kale AA, Torchilin VP. Enhanced transfection of tumor cells in vivo using “Smart” pH-sensitive TAT-modified pegylated liposomes. J Drug Target 2007;15(7-8):538-45
  • Sawant RM, Hurley JP, Salmaso S, et al. “SMART” drug delivery systems: double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjug Chem 2006;17(4):943-9
  • Violini S, Sharma V, Prior JL, et al. Evidence for a plasma membrane-mediated permeability barrier to tat basic domain in well-differentiated epithelial cells: lack of correlation with heparan sulfates. Biochemistry 2002;41(42):12652-61
  • Trehin R, Krauss U, Beck-Sickinger AG, et al. Cellular uptake but low permeation of human calcitonin-derived cell penetrating peptides and Tat(47-57) through well-differentiated epithelial models. Pharm Res 2004;21(7):1248-56
  • Kramer SD, Wunderli-Allenspach H. No entry for TAT(44-57) into liposomes and intact MDCK cells: novel approach to study membrane permeation of cell-penetrating peptides. Biochim Biophys Acta 2003;1609(2):161-9
  • Koch AM, Reynolds F, Merkle HR, et al. Transport of surface-modified nanoparticles through cell monolayers. Chembiochem 2005;6(2):337-45
  • Lindgren ME, Hallbrink MM, Elmquist AM, Langel U. Passage of cell-penetrating peptides across a human epithelial cell layer in vitro. Biochem J 2004;377:69-76
  • Liang JF, Yang VC. Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency. Biochem Biophys Res Commun 2005;335(3):734-8
  • Chen YP, Shen YY, Guo X, et al. Transdermal protein delivery by a coadministered peptide identified via phage display. Nat Biotechnol 2006;24(4):455-60
  • 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(11):1253-7
  • Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004;10(3):310-15

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