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Protein & Peptide Letters

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ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

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Review Article

Development of Cell Penetrating Peptides for Effective Delivery of Recombinant Factors into Target Cells

Author(s): Ubashini Vijakumaran, Fazlina Nordin*, Zariyantey Abdul Hamid, Maha Abdullah and Tye Gee Jun

Volume 27, Issue 11, 2020

Page: [1092 - 1101] Pages: 10

DOI: 10.2174/0929866527666200525164135

Price: $65

Abstract

The cell membrane is a protective layer that strictly controls the passage of molecules restricting the delivery of biomolecules such as drugs, oligonucleotides, peptides, and siRNA into the cells. This shortcoming has been overcome by the discovery of Cell-Penetrating Peptides (CPPs) that has undergone 30 years of evolution. To date, CPPs are largely modified to improve its efficacy and to suit the different delivery applications. The modes of CPPs penetration are still an unresolved mystery and requires further investigations to increase its effectiveness and to diversify its use. Despite having huge potential as a biomolecule carrier, CPPs also have some drawbacks. In this review, the natural and synthetic CPPs, the modifications that have been conducted on CPPs to improve its efficacy, its extended applications, modes of penetration and limitation as well as challenges will be discussed.

Keywords: Cell-penetrating peptide (CPP), cell membrane, biomolecule carrier, protein transduction technology, translocation, recombinant factors.

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[1]
Kalafatovic, D.; Giralt, E. Cell-penetrating peptides: Design strategies beyond primary structure and amphipathicity. Molecules, 2017, 22(11), 1-38.
[http://dx.doi.org/10.3390/molecules22111929] [PMID: 29117144]
[2]
Skotland, T.; Iversen, T.G.; Torgersen, M.L.; Sandvig, K. Cell-penetrating peptides: Possibilities and challenges for drug delivery in vitro and in vivo. Molecules, 2015, 20(7), 13313-13323.
[http://dx.doi.org/10.3390/molecules200713313] [PMID: 26205056]
[3]
Borrelli, A.; Tornesello, A.L.; Tornesello, M.L.; Buonaguro, F.M. Cell penetrating peptides as molecular carriers for anti-cancer agents. Molecules, 2018, 23(2), E295.
[http://dx.doi.org/10.3390/molecules23020295] [PMID: 29385037]
[4]
Gan, B.K.; Yong, C.Y.; Ho, K.L.; Omar, A.R.; Alitheen, N.B.; Tan, W.S. Targeted delivery of cell penetrating peptide virus-like nanoparticles to skin cancer cells. Sci. Rep., 2018, 8(1), 8499.
[http://dx.doi.org/10.1038/s41598-018-26749-y] [PMID: 29855618]
[5]
Chang, X.; Hou, Y. Expression of RecA and cell-penetrating peptide (CPP) fusion protein in bacteria and in mammalian cells. Int. J. Biochem. Mol. Biol., 2018, 9(1), 1-10.
[6]
McClorey, G.; Banerjee, S. Cell-penetrating peptides to enhance delivery of oligonucleotide-based therapeutics. Biomedicines, 2018, 6(2), 51.
[http://dx.doi.org/10.3390/biomedicines6020051] [PMID: 29734750]
[7]
Margus, H.; Padari, K.; Pooga, M. Cell-penetrating peptides as versatile vehicles for oligonucleotide delivery. Mol. Ther., 2012, 20(3), 525-533.
[http://dx.doi.org/10.1038/mt.2011.284] [PMID: 22233581]
[8]
Tai, W.; Gao, X. Functional peptides for siRNA delivery. Adv. Drug Deliv. Rev., 2017, 110-111, 157-168.
[http://dx.doi.org/10.1016/j.addr.2016.08.004] [PMID: 27530388]
[9]
Alhakamy, N.A.; Nigatu, A.S.; Berkland, C.J.; Ramsey, J.D. Noncovalently associated cell-penetrating peptides for gene delivery applications. Ther. Deliv., 2013, 4(6), 741-757.
[http://dx.doi.org/10.4155/tde.13.44] [PMID: 23738670]
[10]
Ding, Y.; Cui, W.; Sun, D.; Wang, G.L.; Hei, Y.; Meng, S.; Chen, J.H.; Xie, Y.; Wang, Z.Q. In vivo study of doxorubicin-loaded cell-penetrating peptide-modified pH-sensitive liposomes: Biocompatibility, bio-distribution, and pharmacodynamics in BALB/c nude mice bearing human breast tumors. Drug Des. Devel. Ther., 2017, 11, 3105-3117.
[http://dx.doi.org/10.2147/DDDT.S149814] [PMID: 29123382]
[11]
Rana, T.M.; Jeang, K.T. Biochemical and functional interactions between HIV-1 Tat protein and TAR RNA. Arch. Biochem. Biophys., 1999, 365(2), 175-185.
[http://dx.doi.org/10.1006/abbi.1999.1206] [PMID: 10328810]
[12]
Garcia, J.A.; Harrich, D.; Soultanakis, E.; Wu, F.; Mitsuyasu, R.; Gaynor, R.B. Human immunodeficiency virus type 1 LTR TATA and TAR region sequences required for transcriptional regulation. EMBO J., 1989, 8(3), 765-778.
[http://dx.doi.org/10.1002/j.1460-2075.1989.tb03437.x] [PMID: 2721501]
[13]
Frankel, A.D.; Pabo, C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 1988, 55(6), 1189-1193.
[http://dx.doi.org/10.1016/0092-8674(88)90263-2] [PMID: 2849510]
[14]
Schwarze, S.R.; Ho, A.; Vocero-Akbani, A.; Dowdy, S.F. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science, 1999, 285(5433), 1569-1572.
[http://dx.doi.org/10.1126/science.285.5433.1569] [PMID: 10477521]
[15]
Maderna, E.; Colombo, L.; Cagnotto, A.; Di Fede, G.; Indaco, A.; Tagliavini, F.; Salmona, M.; Giaccone, G. In situ tissue labeling of cerebral amyloid using HIV-related tat peptide. Mol. Neurobiol., 2018, 55(8), 6834-6840.
[http://dx.doi.org/10.1007/s12035-018-0870-x] [PMID: 29349578]
[16]
Copolovici, D.M.; Langel, K.; Eriste, E.; Langel, Ü. Cell-penetrating peptides: Design, synthesis, and applications. ACS Nano, 2014, 8(3), 1972-1994.
[http://dx.doi.org/10.1021/nn4057269] [PMID: 24559246]
[17]
Derossit, D.; Joliott, M.H.; Chassaingl, G.; Prochiantztn, M. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem., 1994, 269(14), 10444-10450.
[PMID: 8144628]
[18]
Xia, H.; Gao, X.; Gu, G.; Liu, Z.; Hu, Q.; Tu, Y.; Song, Q.; Yao, L.; Pang, Z.; Jiang, X.; Chen, J.; Chen, H. Penetratin-functionalized PEG-PLA nanoparticles for brain drug delivery. Int. J. Pharm., 2012, 436(1-2), 840-850.
[http://dx.doi.org/10.1016/j.ijpharm.2012.07.029] [PMID: 22841849]
[19]
Fischer, P.M.; Zhelev, N.Z.; Wang, S.; Melville, J.E.; Fåhraeus, R.; Lane, D.P. Structure-activity relationship of truncated and substituted analogues of the intracellular delivery vector Penetratin. J. Pept. Res., 2000, 55(2), 163-172.
[http://dx.doi.org/10.1034/j.1399-3011.2000.00163.x] [PMID: 10784032]
[20]
Watson, G.M.; Kulkarni, K.; Brandt, R.; Del Borgo, M.P.; Aguilar, M.I.; Wilce, J.A. Shortened penetratin cell-penetrating peptide is insufficient for cytosolic delivery of a Grb7 targeting peptide. ACS Omega, 2017, 2(2), 670-677.
[http://dx.doi.org/10.1021/acsomega.6b00561] [PMID: 29152602]
[21]
Pooga, M.; Hällbrink, M.; Zorko, M.; Langel, U. Cell penetration by transportan. FASEB J., 1998, 12(1), 67-77.
[http://dx.doi.org/10.1096/fsb2fasebj.12.1.67] [PMID: 9438412]
[22]
Yandek, L.E.; Pokorny, A.; Florén, A.; Knoelke, K.; Langel, U.; Almeida, P.F.F. Mechanism of the cell-penetrating peptide transportan 10 permeation of lipid bilayers. Biophys. J., 2007, 92(7), 2434-2444.
[http://dx.doi.org/10.1529/biophysj.106.100198] [PMID: 17218466]
[23]
Ruczyński, J.; Rusiecka, I.; Turecka, K.; Kozłowska, A.; Alenowicz, M.; Gągało, I.; Kawiak, A.; Rekowski, P.; Waleron, K.; Kocić, I. Transportan 10 improves the pharmacokinetics and pharmacodynamics of vancomycin. Sci. Rep., 2019, 9(1), 1-15.
[http://dx.doi.org/10.1038/s41598-019-40103-w] [PMID: 30626917]
[24]
Aguiar, L.; Machado, M.; Sanches-Vaz, M.; Prudêncio, M.; Vale, N.; Gomes, P. Coupling the cell-penetrating peptides transportan and transportan 10 to primaquine enhances its activity against liver-stage malaria parasites. MedChemComm, 2018, 10(2), 221-226.
[http://dx.doi.org/10.1039/C8MD00447A] [PMID: 30881610]
[25]
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(4), 2437-2443.
[http://dx.doi.org/10.1074/jbc.M110017200] [PMID: 11711547]
[26]
Esposito, C.; Tedeschi, A.; Scrima, M.; D’errico, G.; Ottaviani, M.F.; Rovero, P.; D’ursi, A.M. Exploring interaction of beta-amyloid segment (25-35) with membrane models through paramagnetic probes. J. Pept. Sci., 2006, 12(12), 766-774.
[http://dx.doi.org/10.1002/psc.811] [PMID: 17131288]
[27]
Ter-Avetisyan, G.; Tünnemann, G.; Nowak, D.; Nitschke, M.; Herrmann, A.; Drab, M.; Cardoso, M.C. Cell entry of arginine-rich peptides is independent of endocytosis. J. Biol. Chem., 2009, 284(6), 3370-3378.
[http://dx.doi.org/10.1074/jbc.M805550200] [PMID: 19047062]
[28]
Xu, Y.; Liu, B.R.; Lee, H-J.; Shannon, K.B.; Winiarz, J.G.; Wang, T-C.; Chiang, H-J.; Huang, Y.W. Nona-arginine facilitates delivery of quantum dots into cells via multiple pathways. J. Biomed. Biotechnol., 2010, 2010948543
[http://dx.doi.org/10.1155/2010/948543] [PMID: 21048930]
[29]
Liu, B.R.; Lo, S.Y.; Liu, C.C.; Chyan, C.L.; Huang, Y.W.; Aronstam, R.S.; Lee, H.J. Endocytic trafficking of nanoparticles delivered by cell-penetrating peptides comprised of nona-arginine and a penetration accelerating sequence. PLoS One, 2013, 8(6), e67100.
[http://dx.doi.org/10.1371/journal.pone.0067100] [PMID: 23840594]
[30]
Gautam, A.; Sharma, M.; Vir, P.; Chaudhary, K.; Kapoor, P.; Kumar, R.; Nath, S.K.; Raghava, G.P.S. Identification and characterization of novel protein-derived arginine-rich cell-penetrating peptides. Eur. J. Pharm. Biopharm., 2015, 89(12), 93-106.
[http://dx.doi.org/10.1016/j.ejpb.2014.11.020] [PMID: 25459448]
[31]
Green, M.; Loewenstein, P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell, 1988, 55(6), 1179-1188.
[http://dx.doi.org/10.1016/0092-8674(88)90262-0] [PMID: 2849509]
[32]
Ho, A.; Schwarze, S.R.; Mermelstein, S.J.; Waksman, G.; Dowdy, S.F. Synthetic protein transduction domains: Enhanced transduction potential in vitro and in vivo. Cancer Res., 2001, 61(2), 474-477.
[33]
Mi, Z.; Mai, J.; Lu, X.; Robbins, P.D. Characterization of a class of cationic peptides able to facilitate efficient protein transduction in vitro and in vivo. Mol. Ther., 2000, 2(4), 339-347.
[http://dx.doi.org/10.1006/mthe.2000.0137] [PMID: 11020349]
[34]
Flinterman, M.; Farzaneh, F.; Habib, N.; Malik, F.; Gäken, J.; Tavassoli, M. Delivery of therapeutic proteins as secretable TAT fusion products. Mol. Ther., 2009, 17(2), 334-342.
[http://dx.doi.org/10.1038/mt.2008.256] [PMID: 19050698]
[35]
Denault, J.B.; Leduc, R. Furin/PACE/SPC1: A convertase involved in exocytic and endocytic processing of precursor proteins. FEBS Lett., 1996, 379(2), 113-116.
[http://dx.doi.org/10.1016/0014-5793(95)01487-X] [PMID: 8635573]
[36]
Nordin, F.; Tye, G.J.; Gäken, J.; Farzaneh, F. TATκ fusion protein of OCT-3/4 and KLF-4: Stable mixed population cell lines capable of delivering fusion proteins to target cells. J. Cell Sci. Ther., 2014, 05(02), 5-11.
[37]
Nordin, F.; Abd Hamid, Z.; Vijakumaran, U.; Raja Ahmad, R.N.; Mat Rashid, B. Establishment of stable and secretable TATκ-GFP recombinant protein: A Preliminary report of promoter methylation in 293T cell line. Sains Malays., 2018, 47(10), 2473-2480.
[http://dx.doi.org/10.17576/jsm-2018-4710-24]
[38]
Nordin, F.; Ahmad, R.N.R.; Farzaneh, F. Transactivator protein: An alternative for delivery of recombinant proteins for safer reprogramming of induced Pluripotent Stem Cell. Virus Res., 2017, 235(12), 106-114.
[http://dx.doi.org/10.1016/j.virusres.2017.04.007] [PMID: 28408207]
[39]
Wallbrecher, R.; Ackels, T.; Olea, R.A.; Klein, M.J.; Caillon, L.; Schiller, J.; Bovée-Geurts, P.H.; van Kuppevelt, T.H.; Ulrich, A.S.; Spehr, M.; Adjobo-Hermans, M.J.W.; Brock, R. Membrane permeation of arginine-rich cell-penetrating peptides independent of transmembrane potential as a function of lipid composition and membrane fluidity. J. Control. Release, 2017, 256, 68-78.
[http://dx.doi.org/10.1016/j.jconrel.2017.04.013] [PMID: 28411183]
[40]
Mai, J.C.; Shen, H.; Watkins, S.C.; Cheng, T.; Robbins, P.D. Efficiency of protein transduction is cell type-dependent and is enhanced by dextran sulfate. J. Biol. Chem., 2002, 277(33), 30208-30218.
[http://dx.doi.org/10.1074/jbc.M204202200] [PMID: 12034749]
[41]
Oehlke, J.; Scheller, A.; Wiesner, B.; Krause, E.; Beyermann, M.; Klauschenz, E.; Melzig, M.; Bienert, M. Cellular uptake of an α-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically. Biochim. Biophys. Acta, 1998, 1414(1-2), 127-139.
[http://dx.doi.org/10.1016/S0005-2736(98)00161-8] [PMID: 9804921]
[42]
Simeoni, F.; Morris, M.C.; 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), 2717-2724.
[http://dx.doi.org/10.1093/nar/gkg385] [PMID: 12771197]
[43]
Elliott, G.; Hare, P.O. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell, 1997, 88, 223-233.
[44]
Gabanyi, I.; Lojudice, F.H.; Kossugue, P.M.; Rebelato, E.; Demasi, M.A.; Sogayar, M.C. VP22 herpes simplex virus protein can transduce proteins into stem cells. Braz. J. Med. Biol. Res., 2013, 46(2), 121-127.
[http://dx.doi.org/10.1590/1414-431X20122148] [PMID: 23369972]
[45]
Fernández-Carneado, J.; Kogan, M.J.; Pujals, S.; Giralt, E. Amphipathic peptides and drug delivery. Biopolymers, 2004, 76(2), 196-203.
[http://dx.doi.org/10.1002/bip.10585] [PMID: 15054899]
[46]
Henriques, S.T.; Castanho, M.A.R.B.; Pattenden, L.K.; Aguilar, M-I. Fast membrane association is a crucial factor in the peptide pep-1 translocation mechanism: A kinetic study followed by surface plasmon resonance. Biopolymers, 2010, 94(3), 314-322.
[http://dx.doi.org/10.1002/bip.21367] [PMID: 20049920]
[47]
Lim, J.; Kim, J.; Duong, T.; Lee, G.; Kim, J.; Yoon, J.; Kim, J.; Kim, H.; Ruley, H.E.; El-Rifai, W.; Jo, D. Antitumor activity of cell-permeable p18(INK4c) with enhanced membrane and tissue penetration. Mol. Ther., 2012, 20(8), 1540-1549.
[http://dx.doi.org/10.1038/mt.2012.102] [PMID: 22617107]
[48]
Gao, S.; Simon, M.J.; Hue, C.D.; Morrison, B., III; Banta, S. An unusual cell penetrating peptide identified using a plasmid display-based functional selection platform. ACS Chem. Biol., 2011, 6(5), 484-491.
[http://dx.doi.org/10.1021/cb100423u] [PMID: 21291271]
[49]
Nakayama, F.; Yasuda, T.; Umeda, S.; Asada, M.; Imamura, T.; Meineke, V.; Akashi, M. Fibroblast growth factor-12 (FGF12) translocation into intestinal epithelial cells is dependent on a novel cell-penetrating peptide domain: Involvement of internalization in the in vivo role of exogenous FGF12. J. Biol. Chem., 2011, 286(29), 25823-25834.
[http://dx.doi.org/10.1074/jbc.M110.198267] [PMID: 21518765]
[50]
Murphy, D.J.; Walker, B.; Greer, B.; Harriott, P.; Martin, S.L. A modified Tat peptide for selective intracellular delivery of macromolecules. J. Pharm. Pharmacol., 2011, 63(5), 611-618.
[http://dx.doi.org/10.1111/j.2042-7158.2011.01265.x] [PMID: 21492162]
[51]
Mäe, M.; Langel, U. Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr. Opin. Pharmacol., 2006, 6(5), 509-514.
[http://dx.doi.org/10.1016/j.coph.2006.04.004] [PMID: 16860608]
[52]
Fonseca, S.B.; Pereira, M.P.; Kelley, S.O. Recent advances in the use of cell-penetrating peptides for medical and biological applications. Adv. Drug Deliv. Rev., 2009, 61(11), 953-964.
[http://dx.doi.org/10.1016/j.addr.2009.06.001] [PMID: 19538995]
[53]
Guo, Z.; Peng, H.; Kang, J.; Sun, D. Cell-penetrating peptides: Possible transduction mechanisms and therapeutic applications. Biomed. Rep., 2016, 4(5), 528-534.
[http://dx.doi.org/10.3892/br.2016.639] [PMID: 27123243]
[54]
Madani, F.; Lindberg, S.; Langel, U.; Futaki, S.; Gräslund, A. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 2011, 414729.
[http://dx.doi.org/10.1155/2011/414729] [PMID: 21687343]
[55]
Vivès, 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), 16010-16017.
[http://dx.doi.org/10.1074/jbc.272.25.16010] [PMID: 9188504]
[56]
Rydström, A.; Deshayes, S.; Konate, K.; Crombez, L.; Padari, K.; Boukhaddaoui, H.; Aldrian, G.; Pooga, M.; Divita, G. Direct translocation as major cellular uptake for CADY self-assembling peptide-based nanoparticles. PLoS One, 2011, 6(10), e25924.
[http://dx.doi.org/10.1371/journal.pone.0025924] [PMID: 21998722]
[57]
Deshayes, S.; Gerbal-Chaloin, S.; Morris, M.C.; Aldrian-Herrada, G.; Charnet, P.; Divita, G.; Heitz, F. On the mechanism of non-endosomial peptide-mediated cellular delivery of nucleic acids. Biochim. Biophys. Acta, 2004, 1667(2), 141-147.
[http://dx.doi.org/10.1016/j.bbamem.2004.09.010] [PMID: 15581849]
[58]
Vivès, E.; Schmidt, J.; Pèlegrin, A. Cell-penetrating and cell-targeting peptides in drug delivery. Biochim. Biophys. Acta, 2008, 1786(2), 126-138.
[59]
Herce, H.D.; Garcia, A.E. Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc. Natl. Acad. Sci. USA, 2007, 104(52), 20805-20810.
[http://dx.doi.org/10.1073/pnas.0706574105] [PMID: 18093956]
[60]
Herce, H.D.; Garcia, A.E.; Litt, J.; Kane, R.S.; Martin, P.; Enrique, N.; Rebolledo, A.; Milesi, V. Arginine-rich peptides destabilize the plasma membrane, consistent with a pore formation translocation mechanism of cell-penetrating peptides. Biophys. J., 2009, 97(7), 1917-1925.
[http://dx.doi.org/10.1016/j.bpj.2009.05.066] [PMID: 19804722]
[61]
Jan Akhunzada, M.; Chandramouli, B.; Bhattacharjee, N.; Macchi, S.; Cardarelli, F.; Brancato, G. The role of Tat peptide self-aggregation in membrane pore stabilization: Insights from a computational study. Phys. Chem. Chem. Phys., 2017, 19(40), 27603-27610.
[http://dx.doi.org/10.1039/C7CP05103D] [PMID: 28980686]
[62]
Gao, X.; Hong, S.; Liu, Z.; Yue, T.; Dobnikar, J.; Zhang, X. Membrane potential drives direct translocation of cell-penetrating peptides. Nanoscale, 2019, 11(4), 1949-1958.
[http://dx.doi.org/10.1039/C8NR10447F] [PMID: 30644958]
[63]
Bechara, C.; Sagan, S. Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett., 2013, 587(12), 1693-1702.
[http://dx.doi.org/10.1016/j.febslet.2013.04.031] [PMID: 23669356]
[64]
Prochiantz, A. Getting hydrophilic compounds into cells: Lessons from homeopeptides. Curr. Opin. Neurobiol., 1996, 6(5), 629-634.
[http://dx.doi.org/10.1016/S0959-4388(96)80095-X] [PMID: 8937827]
[65]
Shin, M.C.; Zhang, J.; Min, K.A.; Lee, K.; Byun, Y.; David, A.E.; He, H.; Yang, V.C. Cell-penetrating peptides: Achievements and challenges in application for cancer treatment. J. Biomed. Mater. Res. A, 2014, 102(2), 575-587.
[http://dx.doi.org/10.1002/jbm.a.34859]
[66]
Kawamoto, S.; Takasu, M.; Miyakawa, T.; Morikawa, R.; Oda, T.; Futaki, S.; Nagao, H. Inverted micelle formation of cell-penetrating peptide studied by coarse-grained simulation: Importance of attractive force between cell-penetrating peptides and lipid head group. J. Chem. Phys., 2011, 134(9), 095103.
[http://dx.doi.org/10.1063/1.3555531] [PMID: 21385001]
[67]
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.
[http://dx.doi.org/10.1021/bi00164a017] [PMID: 1463728]
[68]
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. Biophys. J., 2005, 89(6), 4006-4016.
[http://dx.doi.org/10.1529/biophysj.105.068080] [PMID: 16150963]
[69]
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.
[http://dx.doi.org/10.1021/bi960342a] [PMID: 8679603]
[70]
Hirose, H.; Takeuchi, T.; Osakada, H.; Pujals, S.; Katayama, S.; Nakase, I.; Kobayashi, S.; Haraguchi, T.; Futaki, S. Transient focal membrane deformation induced by arginine-rich peptides leads to their direct penetration into cells. Mol. Ther., 2012, 20(5), 984-993.
[http://dx.doi.org/10.1038/mt.2011.313] [PMID: 22334015]
[71]
Derakhshankhah, H.; Jafari, S. Cell penetrating peptides: A concise review with emphasis on biomedical applications. Biomed. Pharmacother., 2018, 108(6), 1090-1096.
[http://dx.doi.org/10.1016/j.biopha.2018.09.097] [PMID: 30372809]
[72]
Jones, A.T. Macropinocytosis: Searching for an endocytic identity and role in the uptake of cell penetrating peptides. J. Cell. Mol. Med., 2007, 11(4), 670-684.
[http://dx.doi.org/10.1111/j.1582-4934.2007.00062.x] [PMID: 17760832]
[73]
Futaki, S.; Nakase, I.; Tadokoro, A.; Takeuchi, T.; Jones, A.T. Arginine-rich peptides and their internalization mechanisms. Biochem. Soc. Trans., 2007, 35(Pt 4), 784-787.
[http://dx.doi.org/10.1042/BST0350784] [PMID: 17635148]
[74]
Mishra, A.; Lai, G.H.; Schmidt, N.W.; Sun, V.Z.; Rodriguez, A.R.; Tong, R.; Tang, L.; Cheng, J.; Deming, T.J.; Kamei, D.T.; Wong, G.C.L. Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions. Proc. Natl. Acad. Sci. USA, 2011, 108(41), 16883-16888.
[http://dx.doi.org/10.1073/pnas.1108795108] [PMID: 21969533]
[75]
Liu, B.R.; Huang, Y.W.; Lee, H.J. Mechanistic studies of intracellular delivery of proteins by cell-penetrating peptides in cyanobacteria. BMC Microbiol., 2013, 13(1), 57.
[http://dx.doi.org/10.1186/1471-2180-13-57] [PMID: 23497160]
[76]
Mayor, S.; Parton, R.G.; Donaldson, J.G. Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol., 2014, 6(6), 1-20.
[http://dx.doi.org/10.1101/cshperspect.a016758] [PMID: 24890511]
[77]
Rousselle, C.; Clair, P.; Lefauconnier, J-M.; Kaczorek, M.; Scherrmann, J-M.; Temsamani, J. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vector-mediated strategy. Mol. Pharmacol., 2000, 57(4), 679-686.
[http://dx.doi.org/10.1124/mol.57.4.679] [PMID: 10727512]
[78]
He, H.; Ye, J.; Liu, E.; Liang, Q.; Liu, Q.; Yang, V.C. Low molecular weight protamine (LMWP): A nontoxic protamine substitute and an effective cell-penetrating peptide. J. Control. Release, 2014, 193, 63-73.
[http://dx.doi.org/10.1016/j.jconrel.2014.05.056] [PMID: 24943246]
[79]
Liu, Z.; Xiong, M.; Gong, J.; Zhang, Y.; Bai, N.; Luo, Y.; Li, L.; Wei, Y.; Liu, Y.; Tan, X.; Xiang, R. Legumain protease-activated TAT-liposome cargo for targeting tumours and their microenvironment. Nat. Commun., 2014, 5, 4280.
[http://dx.doi.org/10.1038/ncomms5280] [PMID: 24969588]
[80]
Kurrikoff, K.; Gestin, M.; Langel, Ü. Recent in vivo advances in cell-penetrating peptide-assisted drug delivery. Expert Opin. Drug Deliv., 2016, 13(3), 373-387.
[http://dx.doi.org/10.1517/17425247.2016.1125879] [PMID: 26634750]
[81]
Fomby, P.; Cherlin, A.J. Nanopreparations for organelle-specific delivery in cancer. Adv. Drug Deliv. Rev., 2011, 72(2), 181-204.
[82]
de Oliveira-Mendes, B.B.R.; Horta, C.C.R.; do Carmo, A.O.; Biscoto, G.L.; Sales-Medina, D.F.; Leal, H.G.; Brandão-Dias, P.F.P.; Miranda, S.E.M.; Aguiar, C.J.; Cardoso, V.N.; de Barros, A.L.B.; Chávez-Olortégui, C.; Leite, M.F.; Kalapothakis, E. CPP-Ts: A new intracellular calcium channel modulator and a promising tool for drug delivery in cancer cells. Sci. Rep., 2018, 8(1), 1-13.
[http://dx.doi.org/10.1038/s41598-018-33133-3] [PMID: 29311619]
[83]
Wei, Y.; Ma, L.; Zhang, L.; Xu, X. Noncovalent interaction-assisted drug delivery system with highly efficient uptake and release of paclitaxel for anticancer therapy. Int. J. Nanomedicine, 2017, 12, 7039-7051.
[http://dx.doi.org/10.2147/IJN.S144322] [PMID: 29026300]
[84]
Jiang, T.; Wang, T.; Li, T.; Ma, Y.; Shen, S.; He, B.; Mo, R. Enhanced transdermal drug delivery by transfersome-embedded oligopeptide hydrogel for topical chemotherapy of melanoma. ACS Nano, 2018, 12(10), 9693-9701.
[http://dx.doi.org/10.1021/acsnano.8b03800] [PMID: 30183253]
[85]
Tian, J.; Min, Y.; Rodgers, Z.; Wan, X.; Qiu, H.; Mi, Y.; Tian, X.; Wagner, K.T.; Caster, J.M.; Qi, Y.; Roche, K.; Zhang, T.; Cheng, J.; Wang, A.Z. Nanoparticle delivery of chemotherapy combination regimen improves the therapeutic efficacy in mouse models of lung cancer. Nanomedicine (Lond.), 2017, 13(3), 1301-1307.
[http://dx.doi.org/10.1016/j.nano.2016.11.007] [PMID: 27884641]
[86]
Kurrikoff, K.; Veiman, K.; Künnapuu, K.; Peets, E.M.; Lehto, T. Effective in vivo gene delivery with reduced toxicity, achieved by charge and fatty acid -modified cell penetrating peptide. Sci. Rep., 2017, 11, 1-11.
[http://dx.doi.org/10.1038/s41598-017-17316-y]
[87]
Osman, G.; Rodriguez, J.; Chan, S.Y.; Chisholm, J.; Duncan, G.; Kim, N.; Tatler, A.L.; Shakesheff, K.M.; Hanes, J.; Suk, J.S.; Dixon, J.E. PEGylated enhanced cell penetrating peptide nanoparticles for lung gene therapy. J. Control. Release, 2018, 285, 35-45.
[http://dx.doi.org/10.1016/j.jconrel.2018.07.001] [PMID: 30004000]
[88]
Kanasty, R.; Dorkin, J.R.; Vegas, A.; Anderson, D. Delivery materials for siRNA therapeutics. Nat. Mater., 2013, 12(11), 967-977.
[http://dx.doi.org/10.1038/nmat3765] [PMID: 24150415]
[89]
Tatiparti, K.; Sau, S.; Kashaw, S.K.; Iyer, A.K. siRNA delivery strategies: A comprehensive review of recent developments. Nanomaterials (Basel), 2017, 7(4), 77.
[http://dx.doi.org/10.3390/nano7040077] [PMID: 28379201]
[90]
Wang, Y.H.; Hou, Y.W.; Lee, H.J. An intracellular delivery method for siRNA by an arginine-rich peptide. J. Biochem. Biophys. Methods, 2007, 70(4), 579-586.
[http://dx.doi.org/10.1016/j.jbbm.2007.01.010] [PMID: 17320189]
[91]
Aldrian, G.; Vaissière, A.; Konate, K.; Seisel, Q.; Vivès, E.; Fernandez, F.; Viguier, V.; Genevois, C.; Couillaud, F.; Démèné, H.; Aggad, D.; Covinhes, A.; Barrère-Lemaire, S.; Deshayes, S.; Boisguerin, P. PEGylation rate influences peptide-based nanoparticles mediated siRNA delivery in vitro and in vivo. J. Control. Release, 2017, 256, 79-91.
[http://dx.doi.org/10.1016/j.jconrel.2017.04.012] [PMID: 28411182]
[92]
Ullah, I.; Chung, K.; Beloor, J.; Kim, J.; Cho, M.; Kim, N.; Lee, K.Y.; Kumar, P.; Lee, S.K. Trileucine residues in a ligand-CPP-based siRNA delivery platform improve endosomal escape of siRNA. J. Drug Target., 2017, 25(4), 320-329.
[http://dx.doi.org/10.1080/1061186X.2016.1258566] [PMID: 27820977]
[93]
Xiang, B.; Jia, X.L.; Qi, J.L.; Yang, L.P.; Sun, W.H.; Yan, X.; Yang, S.K.; Cao, D.Y.; Du, Q.; Qi, X.R. Enhancing siRNA-based cancer therapy using a new pH-responsive activatable cell-penetrating peptide-modified liposomal system. Int. J. Nanomedicine, 2017, 12, 2385-2405.
[http://dx.doi.org/10.2147/IJN.S129574] [PMID: 28405163]
[94]
Nielsen, E.J.B.; Yoshida, S.; Kamei, N.; Iwamae, R.; Khafagy, S.; Olsen, J.; Rahbek, U.L.; Pedersen, B.L.; Takayama, K.; Takeda-Morishita, M. In vivo proof of concept of oral insulin delivery based on a co-administration strategy with the cell-penetrating peptide penetratin. J. Control. Release, 2014, 189, 19-24.
[http://dx.doi.org/10.1016/j.jconrel.2014.06.022] [PMID: 24973720]
[95]
Ul Ain, Q.; Lee, J.H.; Woo, Y.S.; Kim, Y.H. Effects of protein transduction domain (PTD) selection and position for improved intracellular delivery of PTD-Hsp27 fusion protein formulations. Arch. Pharm. Res., 2016, 39(9), 1266-1274.
[http://dx.doi.org/10.1007/s12272-016-0786-9] [PMID: 27381220]
[96]
Dinca, A.; Chien, W.M.; Chin, M.T. Intracellular delivery of proteins with cell-penetrating peptides for therapeutic uses in human disease. Int. J. Mol. Sci., 2016, 17(2), 263.
[http://dx.doi.org/10.3390/ijms17020263] [PMID: 26907261]

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