Login Register Cart 0
Review Article

Cell-penetrating Peptide-mediated Nanovaccine Delivery

Author(s): Jizong Jiang*

Volume 22, Issue 8, 2021

Published on: 03 February, 2021

Page: [896 - 912] Pages: 17

DOI: 10.2174/1389450122666210203193225

Price: $65

Abstract

Vaccination with small antigens, such as proteins, peptides, or nucleic acids, is used to activate the immune system and trigger the protective immune responses against a pathogen. Currently, nanovaccines are undergoing development instead of conventional vaccines. The size of nanovaccines is in the range of 10-500 nm, which enables them to be readily taken up by cells and exhibit improved safety profiles. However, low-level immune responses, as the removal of redundant pathogens, trigger counter-effective activation of the immune system invalidly and present a challenging obstacle to antigen recognition and its uptake via antigen-presenting cells (APCs). In addition, toxicity can be substantial. To overcome these problems, a variety of cell-penetrating peptide (CPP)-mediated vaccine delivery systems based on nanotechnology have been proposed, most of which are designed to improve the stability of antigens in vivo and their delivery into immune cells. CPPs are particularly attractive components of antigen delivery. Thus, the unique translocation property of CPPs ensures that they remain an attractive carrier with the capacity to deliver cargo in an efficient manner for the application of drugs, gene transfer, protein, and DNA/RNA vaccination delivery. CPP-mediated nanovaccines can enhance antigen uptake, processing, and presentation by APCs, which are the fundamental steps in initiating an immune response. This review describes the different types of CPP-based nanovaccines delivery strategies.

Keywords: Cell-penetrating peptide, nanoparticle, vaccine, immune response, delivery system, nanotechnology.

« Previous Next »
Graphical Abstract

[1]
Alonso PL, Tanner M. Public health challenges and prospects for malaria control and elimination. Nat Med 2013; 19(2): 150-5.
[http://dx.doi.org/10.1038/nm.3077] [PMID: 23389615]
[2]
Alm JS, Lilja G, Pershagen G, Scheynius A. Early BCG vaccination and development of atopy. Lancet 1997; 350(9075): 400-3.
[http://dx.doi.org/10.1016/S0140-6736(97)02207-1] [PMID: 9259654]
[3]
Bull JJ. Evolutionary reversion of live viral vaccines: Can genetic engineering subdue it? Virus Evol 2015; 1(1): vev005.
[http://dx.doi.org/10.1093/ve/vev005] [PMID: 27034780]
[4]
Baxter D. Active and passive immunity, vaccine types, excipients and licensing. Occup Med (Lond) 2007; 57(8): 552-6.
[http://dx.doi.org/10.1093/occmed/kqm110] [PMID: 18045976]
[5]
Singh M, O’Hagan D. Advances in vaccine adjuvants. Nat Biotechnol 1999; 17(11): 1075-81.
[http://dx.doi.org/10.1038/15058] [PMID: 10545912]
[6]
Glenny AT, Pope CG, Waddington H, et al. Immunological notes. XVII–XXIV. J Pathol Bacteriol 1926; 29: 31-40.
[http://dx.doi.org/10.1002/path.1700290106]
[7]
Opie EL, Freund J. An experimental study of protective inoculation with heat killed tubercle bacilli. J Exp Med 1937; 66(6): 761-88.
[http://dx.doi.org/10.1084/jem.66.6.761] [PMID: 19870697]
[8]
Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55(6): 1189-93.
[http://dx.doi.org/10.1016/0092-8674(88)90263-2] [PMID: 2849510]
[9]
Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 1988; 55(6): 1179-88.
[http://dx.doi.org/10.1016/0092-8674(88)90262-0] [PMID: 2849509]
[10]
Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994; 269(14): 10444-50.
[PMID: 8144628]
[11]
Vasconcelos L, Pärn K, Langel U. Therapeutic potential of cell-penetrating peptides. Ther Deliv 2013; 4(5): 573-91.
[http://dx.doi.org/10.4155/tde.13.22] [PMID: 23647276]
[12]
Martin ME, Rice KG. Peptide-guided gene delivery. AAPS J 2007; 9(1): E18-29.
[http://dx.doi.org/10.1208/aapsj0901003] [PMID: 17408236]
[13]
Sawant R, Torchilin V. Intracellular transduction using cell-penetrating peptides. Mol Biosyst 2010; 6(4): 628-40.
[http://dx.doi.org/10.1039/B916297F] [PMID: 20237640]
[14]
Qian Z, Dougherty PG, Pei D. Monitoring the cytosolic entry of cell-penetrating peptides using a pH-sensitive fluorophore. Chem Commun (Camb) 2015; 51(11): 2162-5.
[http://dx.doi.org/10.1039/C4CC09441G] [PMID: 25554998]
[15]
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.
[http://dx.doi.org/10.1016/j.bcp.2005.10.048] [PMID: 16376307]
[16]
Margus H, Padari K, Pooga M. Cell-penetrating peptides as versatile vehicles for oligonucleotide delivery. Mol Ther 2012; 20(3): 525-33.
[http://dx.doi.org/10.1038/mt.2011.284] [PMID: 22233581]
[17]
Morris MC, Depollier J, Mery J, Heitz F, Divita G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 2001; 19(12): 1173-6.
[http://dx.doi.org/10.1038/nbt1201-1173] [PMID: 11731788]
[18]
Deshayes S, Morris MC, Divita G, Heitz F. Cell-penetrating peptides: tools for intracellular delivery of therapeutics. Cell Mol Life Sci 2005; 62(16): 1839-49.
[http://dx.doi.org/10.1007/s00018-005-5109-0] [PMID: 15968462]
[19]
Galdiero S, Falanga A, Vitiello M, et al. Exploitation of viral properties for intracellular delivery. J Pept Sci 2014; 20(7): 468-78.
[http://dx.doi.org/10.1002/psc.2649] [PMID: 24889153]
[20]
Skwarczynski M, Toth I. Cell-penetrating peptides in vaccine delivery: facts, challenges and perspectives. Ther Deliv 2019; 10(8): 465-7.
[http://dx.doi.org/10.4155/tde-2019-0042] [PMID: 31462173]
[21]
Liu F, Shollenberger LM, Conwell CC, Yuan X, Huang L. Mechanism of naked DNA clearance after intravenous injection. J Gene Med 2007; 9(7): 613-9.
[http://dx.doi.org/10.1002/jgm.1054] [PMID: 17534886]
[22]
Lai E, van Zanten JH. Evidence of lipoplex dissociation in liquid formulations. J Pharm Sci 2002; 91(5): 1225-32.
[http://dx.doi.org/10.1002/jps.10108] [PMID: 11977098]
[23]
Lv H, Zhang S, Wang B, Cui S, Yan J. Toxicity of cationic lipids and cationic polymers in gene delivery. J Control Release 2006; 114(1): 100-9.
[http://dx.doi.org/10.1016/j.jconrel.2006.04.014] [PMID: 16831482]
[24]
Bolhassani A, Safaiyan S, Rafati S. Improvement of different vaccine delivery systems for cancer therapy. Mol Cancer 2011; 10: 3.
[http://dx.doi.org/10.1186/1476-4598-10-3] [PMID: 21211062]
[25]
Liu Y, Chen C. Role of nanotechnology in HIV/AIDS vaccine development. Adv Drug Deliv Rev 2016; 103: 76-89.
[http://dx.doi.org/10.1016/j.addr.2016.02.010] [PMID: 26952542]
[26]
Ahmed TA, Aljaeid BM. Preparation, characterization, and potential application of chitosan, chitosan derivatives, and chitosan metal nanoparticles in pharmaceutical drug delivery. Drug Des Devel Ther 2016; 10: 483-507.
[http://dx.doi.org/10.2147/DDDT.S99651] [PMID: 26869768]
[27]
Sun B, Xia T. Nanomaterial-based vaccine adjuvants. J Mater Chem B Mater Biol Med 2016; 4(33): 5496-509.
[http://dx.doi.org/10.1039/C6TB01131D] [PMID: 30774955]
[28]
Hu Y, Hoerle R, Ehrich M, Zhang C. Engineering the lipid layer of lipid-PLGA hybrid nanoparticles for enhanced in vitro cellular uptake and improved stability. Acta Biomater 2015; 28: 149-59.
[http://dx.doi.org/10.1016/j.actbio.2015.09.032] [PMID: 26428192]
[29]
Wang X, Yang D, Li S, Xu X, Qin CF, Tang R. Biomineralized vaccine nanohybrid for needle-free intranasal immunization. Biomaterials 2016; 106: 286-94.
[http://dx.doi.org/10.1016/j.biomaterials.2016.08.035] [PMID: 27575530]
[30]
Klippstein R, Pozo D. Nanotechnology-based manipulation of dendritic cells for enhanced immunotherapy strategies. Nanomedicine (Lond) 2010; 6(4): 523-9.
[http://dx.doi.org/10.1016/j.nano.2010.01.001] [PMID: 20085824]
[31]
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.
[http://dx.doi.org/10.1080/10611860701498203] [PMID: 17671900]
[32]
Maiolo JR, Ferrer M, Ottinger EA. Effects of cargo molecules on the cellular uptake of arginine-rich cell-penetrating peptides. Biochim Biophys Acta 2005; 1712(2): 161-72.
[http://dx.doi.org/10.1016/j.bbamem.2005.04.010] [PMID: 15935328]
[33]
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 1996; 271(30): 18188-93.
[http://dx.doi.org/10.1074/jbc.271.30.18188] [PMID: 8663410]
[34]
Sokolov Y, Mirzabekov T, Martin DW, Lehrer RI, Kagan BL. Membrane channel formation by antimicrobial protegrins. Biochim Biophys Acta 1999; 1420(1-2): 23-9.
[http://dx.doi.org/10.1016/S0005-2736(99)00086-3] [PMID: 10446287]
[35]
Koren E, Apte A, Sawant RR, Grunwald J, Torchilin VP. Cell-penetrating TAT peptide in drug delivery systems: proteolytic stability requirements. Drug Deliv 2011; 18(5): 377-84.
[http://dx.doi.org/10.3109/10717544.2011.567310] [PMID: 21438724]
[36]
Marasini N, Giddam AK, Batzloff MR, et al. Poly-L-lysine-coated nanoparticles are ineffective in inducing mucosal immunity against group a streptococcus. Bio Chem Comp 2017; 5: 1-6.
[http://dx.doi.org/10.7243/2052-9341-5-1]
[37]
Tang J, Yin R, Tian Y, et al. A novel self-assembled nanoparticle vaccine with HIV-1 Tat (49-57)/HPV16 E7(49-57) fusion peptide and GM-CSF DNA elicits potent and prolonged CD8(+) T cell-dependent anti-tumor immunity in mice. Vaccine 2012; 30(6): 1071-82.
[http://dx.doi.org/10.1016/j.vaccine.2011.12.029] [PMID: 22178528]
[38]
Mohri K, Miyata K, Egawa T, et al. Effects of the chemical structures of oligoarginines conjugated to biocompatible polymers as a mucosal adjuvant on antibody induction in nasal cavities. Chem Pharm Bull (Tokyo) 2018; 66(4): 375-81.
[http://dx.doi.org/10.1248/cpb.c17-00834] [PMID: 29607903]
[39]
Schutze-Redelmeier MPM, Kong S, Bally MB, Dutz JP. Antennapedia transduction sequence promotes anti tumour immunity to epicutaneously administered CTL epitopes. Vaccine 2004; 22(15-16): 1985-91.
[http://dx.doi.org/10.1016/j.vaccine.2003.10.028] [PMID: 15121311]
[40]
Deshayes S, Plénat T, Aldrian-Herrada G, Divita G, Le Grimellec C, Heitz F. Primary amphipathic cell-penetrating peptides: structural requirements and interactions with model membranes. Biochemistry 2004; 43(24): 7698-706.
[http://dx.doi.org/10.1021/bi049298m] [PMID: 15196012]
[41]
Yu X, Wang Y, Xia Y, Zhang L, Yang Q, Lei J. A DNA vaccine encoding VP22 of herpes simplex virus type I (HSV-1) and OprF confers enhanced protection from Pseudomonas aeruginosa in mice. Vaccine 2016; 34(37): 4399-405.
[http://dx.doi.org/10.1016/j.vaccine.2016.07.017] [PMID: 27449680]
[42]
Mardani G, Bolhassani A, Agi E, Shahbazi S, Mehdi Sadat S. Protein vaccination with HPV16 E7/Pep-1 nanoparticles elicits a protective T-helper cell-mediated immune response. IUBMB Life 2016; 68(6): 459-67.
[http://dx.doi.org/10.1002/iub.1503] [PMID: 27094221]
[43]
Pujals S, Giralt E. Proline-rich, amphipathic cell-penetrating peptides. Adv Drug Deliv Rev 2008; 60(4-5): 473-84.
[http://dx.doi.org/10.1016/j.addr.2007.09.012] [PMID: 18187229]
[44]
Kardani K, Milani A, H Shabani S, Bolhassani A. Cell penetrating peptides: the potent multi-cargo intracellular carriers. Expert Opin Drug Deliv 2019; 16(11): 1227-58.
[http://dx.doi.org/10.1080/17425247.2019.1676720] [PMID: 31583914]
[45]
Veach RA, Liu D, Yao S, et al. Receptor/transporter-independent targeting of functional peptides across the plasma membrane. J Biol Chem 2004; 279(12): 11425-31.
[http://dx.doi.org/10.1074/jbc.M311089200] [PMID: 14699109]
[46]
Mayor S, Parton RG, Donaldson JG. 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]
[47]
Yang J, Luo Y, Shibu MA, Toth I, Skwarczynskia M. Cell-penetrating peptides: efficient vectors for vaccine delivery. Curr Drug Deliv 2019; 16(5): 430-43.
[http://dx.doi.org/10.2174/1567201816666190123120915] [PMID: 30760185]
[48]
Mai JC, Shen H, Watkins SC, Cheng T, Robbins PD. Efficiency of protein transduction is cell type-dependent and is enhanced by dextran sulfate. J Biol Chem 2002; 277(33): 30208-18.
[http://dx.doi.org/10.1074/jbc.M204202200] [PMID: 12034749]
[49]
Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 1999; 17: 593-623.
[http://dx.doi.org/10.1146/annurev.immunol.17.1.593] [PMID: 10358769]
[50]
Hillaireau H, Couvreur P. Nanocarriers’ entry into the cell: relevance to drug delivery. Cell Mol Life Sci 2009; 66(17): 2873-96.
[http://dx.doi.org/10.1007/s00018-009-0053-z] [PMID: 19499185]
[51]
Maniti O, Piao HR, Ayala-Sanmartin J. Basic cell penetrating peptides induce plasma membrane positive curvature, lipid domain separation and protein redistribution. Int J Biochem Cell Biol 2014; 50: 73-81.
[http://dx.doi.org/10.1016/j.biocel.2014.02.017] [PMID: 24583633]
[52]
Tali C. Scavenger receptors as a target for nucleic acid delivery with peptide vectors. University of Tarita Press 2017.
[53]
Ván ová J, Hejtmánková AT, Kalbác ová MH. The utilization of cell-penetrating peptides in the intracellular delivery of viral nanoparticles. Materials 2019; 12: 2671.
[54]
Winkler J. Nanomedicines based on recombinant fusion proteins for targeting therapeutic siRNA oligonucleotides. Ther Deliv 2011; 2(7): 891-905.
[http://dx.doi.org/10.4155/tde.11.56] [PMID: 22318893]
[55]
Kim H, Seo EH, Lee SH, Kim BJ. The telomerase-derived anticancer peptide vaccine GV1001 as an extracellular heat shock protein-mediated cell-penetrating peptide. Int J Mol Sci 2016; 17(12): 2054.
[http://dx.doi.org/10.3390/ijms17122054] [PMID: 27941629]
[56]
Lee SA, Kim BR, Kim BK, et al. Heat shock protein-mediated cell penetration and cytosolic delivery of macromolecules by a telomerase-derived peptide vaccine. Biomaterials 2013; 34(30): 7495-505.
[http://dx.doi.org/10.1016/j.biomaterials.2013.06.015] [PMID: 23827187]
[57]
Wang RF, Wang HY. Enhancement of antitumor immunity by prolonging antigen presentation on dendritic cells. Nat Biotechnol 2002; 20(2): 149-54.
[http://dx.doi.org/10.1038/nbt0202-149] [PMID: 11821860]
[58]
Seesuay W, Jittavisutthikul S, Sae-Lim N, Sookrung N, Sakolvaree Y, Chaicumpa W. Human transbodies that interfere with the functions of Ebola virus VP35 protein in genome replication and transcription and innate immune antagonism. Emerg Microbes Infect 2018; 7(1): 41.
[http://dx.doi.org/10.1038/s41426-018-0031-3] [PMID: 29568066]
[59]
Lim S, Koo JH, Choi JM. Use of cell-penetrating peptides in dendritic cell-based vaccination. Immune Netw 2016; 16(1): 33-43.
[http://dx.doi.org/10.4110/in.2016.16.1.33] [PMID: 26937230]
[60]
Al-Husaini K, Elkamel E, Han XX, et al. Therapeutic potential of a cell penetrating peptide (CPP, NP1) mediated siRNA delivery: Evidence in 3D spheroids of colon cancer cells. Can J Chem Eng 2020; 98: 1240-54.
[http://dx.doi.org/10.1002/cjce.23743]
[61]
Davoodi S, Bolhassani A, Sadat SM, Irani S. Design and in vitro delivery of HIV-1 multi-epitope DNA and peptide constructs using novel cell-penetrating peptides. Biotechnol Lett 2019; 41(11): 1283-98.
[http://dx.doi.org/10.1007/s10529-019-02734-x] [PMID: 31531750]
[62]
Muto K, Kamei N, Yoshida M, Takayama K, Takeda-Morishita M. Cell-penetrating peptide penetratin as a potential tool for developing effective nasal vaccination systems. J Pharm Sci 2016; 105(6): 2014-7.
[http://dx.doi.org/10.1016/j.xphs.2016.03.026] [PMID: 27155764]
[63]
Alizadeh S, Irani S, Bolhassani A, Sadat SM. Simultaneous use of natural adjuvants and cell penetrating peptides improves HCV NS3 antigen-specific immune responses. Immunol Lett 2019; 212: 70-80.
[http://dx.doi.org/10.1016/j.imlet.2019.06.011] [PMID: 31254535]
[64]
Shahbazi S, Bolhassani A. Comparison of six cell penetrating peptides with different properties for in vitro and in vivo delivery of HPV16 E7 antigen in therapeutic vaccines. Int Immunopharmacol 2018; 62: 170-80.
[http://dx.doi.org/10.1016/j.intimp.2018.07.006] [PMID: 30015237]
[65]
Lam P, Steinmetz NF. Delivery of siRNA therapeutics using cowpea chlorotic mottle virus-like particles. Biomater Sci 2019; 7(8): 3138-42.
[http://dx.doi.org/10.1039/C9BM00785G] [PMID: 31257379]
[66]
Zhang TT, Kang TH, Ma B, Xu Y, Hung CF, Wu TC. LAH4 enhances CD8+ T cell immunity of protein/peptide-based vaccines. Vaccine 2012; 30(4): 784-93.
[http://dx.doi.org/10.1016/j.vaccine.2011.11.056] [PMID: 22120194]
[67]
Shi XG, Song HJ, Wang CG, et al. Co-assembled and self-delivered epitope/CpG nanocomplex vaccine T augments peptide immunogenicity for cancer immunotherapy. Chem Eng J 2020; 399: 125854.
[http://dx.doi.org/10.1016/j.cej.2020.125854]
[68]
Mehrlatifan S, Mirnurollahi SM, Motevalli F, Rahimi P, Soleymani S, Bolhassani A. The structural HCV genes delivered by MPG cell penetrating peptide are directed to enhance immune responses in mice model. Drug Deliv 2016; 23(8): 2852-9.
[http://dx.doi.org/10.3109/10717544.2015.1108375] [PMID: 26559939]
[69]
Fang WB, Yao M, Brummer G, et al. Targeted gene silencing of CCL2 inhibits triple negative breast cancer progression by blocking cancer stem cell renewal and M2 macrophage recruitment. Oncotarget 2016; 7(31): 49349-67.
[http://dx.doi.org/10.18632/oncotarget.9885] [PMID: 27283985]
[70]
Sun Y, Hu YH. Cell-penetrating peptide-mediated subunit vaccine generates a potent immune response and protection against Streptococcus iniae in Japanese flounder (Paralichthys olivaceus). Vet Immunol Immunopathol 2015; 167(3-4): 96-103.
[http://dx.doi.org/10.1016/j.vetimm.2015.07.008] [PMID: 26232860]
[71]
Ma J, Xu J, Guan L, et al. Cell-penetrating peptides mediated protein cross-membrane delivery and its use in bacterial vector vaccine. Fish Shellfish Immunol 2014; 39(1): 8-16.
[http://dx.doi.org/10.1016/j.fsi.2014.04.003] [PMID: 24746937]
[72]
Granadillo M, Vallespi MG, Batte A, et al. A novel fusion protein-based vaccine comprising a cell penetrating and immunostimulatory peptide linked to human papillomavirus (HPV) type 16 E7 antigen generates potent immunologic and anti-tumor responses in mice. Vaccine 2011; 29(5): 920-30.
[http://dx.doi.org/10.1016/j.vaccine.2010.11.083] [PMID: 21145912]
[73]
Yanez RJR, Lamprecht R, Granadillo M, et al. Expression optimization of a cell membrane-penetrating human papillomavirus type 16 therapeutic vaccine candidate in Nicotiana benthamiana. PLoS One 2017; 12(8): e0183177.
[http://dx.doi.org/10.1371/journal.pone.0183177] [PMID: 28800364]
[74]
Alfonso AB, Granadillo M, Batte A, et al. Biological activity of LALF32-51–E7, a vaccine candidate for the treatment of anogenital lesions associated to HPV16. J Cell Immun 2018; 4: 71-4.
[http://dx.doi.org/10.1016/j.jocit.2018.07.001]
[75]
Derouazi M, Di Berardino-Besson W, Belnoue E, et al. Novel cell-penetrating peptide-based vaccine induces robust CD4 and CD8 T cell–mediated antitumor immunity. Cancer Res 2015; 75(15): 3020-31.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-3017] [PMID: 26116496]
[76]
Jagot-Lacoussiere L, Kotula E, Villoutreix BO, Bruzzoni-Giovanelli H, Poyet JL. A cell-penetrating peptide targeting AAC-11 specifically induces cancer cells death. Cancer Res 2016; 76(18): 5479-90.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-0302] [PMID: 27406828]
[77]
Endoh T, Sisido M, Ohtsuki T. Cellular siRNA delivery mediated by a cell-permeant RNA-binding protein and photoinduced RNA interference. Bioconjug Chem 2008; 19(5): 1017-24.
[http://dx.doi.org/10.1021/bc800020n] [PMID: 18442282]
[78]
Bleifuss E, Kammertoens T, Hutloff A, et al. The translocation motif of hepatitis B virus improves protein vaccination. Cell Mol Life Sci 2006; 63(5): 627-35.
[http://dx.doi.org/10.1007/s00018-005-5548-7] [PMID: 16482397]
[79]
Rostami B, Irani S, Bolhassani A, Cohan RA. Gene and protein delivery using four cell penetrating peptides for HIV-1 vaccine development. IUBMB Life 2019; 71(10): 1619-33.
[http://dx.doi.org/10.1002/iub.2107] [PMID: 31220406]
[80]
Saleh T, Bolhassani A, Shojaosadati SA, Aghasadeghi MR. MPG-based nanoparticle: An efficient delivery system for enhancing the potency of DNA vaccine expressing HPV16E7. Vaccine 2015; 33(28): 3164-70.
[http://dx.doi.org/10.1016/j.vaccine.2015.05.015] [PMID: 26001433]
[81]
Fuenmayor J, Gòdia F, Cervera L. Production of virus-like particles for vaccines. N Biotechnol 2017; 39(Pt B): 174-80.
[http://dx.doi.org/10.1016/j.nbt.2017.07.010] [PMID: 28778817]
[82]
Riley MK, Vermerris W. Recent advances in nanomaterials for gene delivery—a review. Nanomaterials (Basel) 2017; 7(5): 94.
[http://dx.doi.org/10.3390/nano7050094] [PMID: 28452950]
[83]
Bolhassani A, Jafarzade BS, Mardani G. In vitro and in vivo delivery of therapeutic proteins using cell penetrating peptides. Peptides 2017; 87: 50-63.
[http://dx.doi.org/10.1016/j.peptides.2016.11.011] [PMID: 27887988]
[84]
Takenobu T, Tomizawa K, Matsushita M, et al. Development of p53 protein transduction therapy using membrane-permeable peptides and the application to oral cancer cells. Mol Cancer Ther 2002; 1(12): 1043-9.
[PMID: 12481427]
[85]
Sun Y, Sun Y, Zhao R, Gao K. Intracellular delivery of messenger RNA by recombinant PP7 virus-like particles carrying low molecular weight protamine. BMC Biotechnol 2016; 16(1): 46.
[http://dx.doi.org/10.1186/s12896-016-0274-9] [PMID: 27233770]
[86]
Pan Y, Zhang Y, Jia T, Zhang K, Li J, Wang L. Development of a microRNA delivery system based on bacteriophage MS2 virus-like particles. FEBS J 2012; 279(7): 1198-208.
[http://dx.doi.org/10.1111/j.1742-4658.2012.08512.x] [PMID: 22309233]
[87]
Lee HB, Yoon SY, Singh B, et al. Oral immunization of FMDV vaccine using pH-sensitive and mucoadhesive thiolated cellulose acetate phthalate microparticles. Tissue Eng Regen Med 2017; 15(1): 1-11.
[http://dx.doi.org/10.1007/s13770-017-0082-x] [PMID: 30603530]
[88]
Petrovsky N. Comparative safety of vaccine adjuvants: A summary of current evidence and future Needs. Drug Saf 2015; 38(11): 1059-74.
[http://dx.doi.org/10.1007/s40264-015-0350-4] [PMID: 26446142]
[89]
Erazo-Oliveras A, Muthukrishnan N, Baker R, Wang TY, Pellois JP. Improving the endosomal escape of cell-penetrating peptides and their cargos: strategies and challenges. Pharmaceuticals (Basel) 2012; 5(11): 1177-209.
[http://dx.doi.org/10.3390/ph5111177] [PMID: 24223492]
[90]
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.
[http://dx.doi.org/10.1074/jbc.M209548200] [PMID: 12411431]
[91]
Vijayan V, Mohapatra A, Uthaman S, et al. Improving the endosomal escape of cell-penetrating peptides and their cargos: strategies and challenges. Pharmaceutics 2019; 11: 534.
[http://dx.doi.org/10.3390/pharmaceutics11100534]
[92]
Wang J, Hu X, Xiang D. Nanoparticle drug delivery systems: an excellent carrier for tumor peptide vaccines. Drug Deliv 2018; 25(1): 1319-27.
[http://dx.doi.org/10.1080/10717544.2018.1477857] [PMID: 29869539]
[93]
Müller LK, Landfester K. Natural liposomes and synthetic polymeric structures for biomedical applications. Biochem Biophys Res Commun 2015; 468(3): 411-8.
[http://dx.doi.org/10.1016/j.bbrc.2015.08.088] [PMID: 26315266]
[94]
Schroeder A, Levins CG, Cortez C, Langer R, Anderson DG. Lipid-based nanotherapeutics for siRNA delivery. J Intern Med 2010; 267(1): 9-21.
[http://dx.doi.org/10.1111/j.1365-2796.2009.02189.x] [PMID: 20059641]
[95]
Tseng YL, Liu JJ, Hong RL. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol Pharmacol 2002; 62(4): 864-72.
[http://dx.doi.org/10.1124/mol.62.4.864] [PMID: 12237333]
[96]
Fretz MM, Koning GA, Mastrobattista E, Jiskoot W, Storm G. OVCAR-3 cells internalize TAT-peptide modified liposomes by endocytosis. Biochim Biophys Acta 2004; 1665(1-2): 48-56.
[http://dx.doi.org/10.1016/j.bbamem.2004.06.022] [PMID: 15471570]
[97]
Torchilin VP. Cell penetrating peptide-modified pharmaceutical nanocarriers for intracellular drug and gene delivery. Biopolymers 2008; 90(5): 604-10.
[http://dx.doi.org/10.1002/bip.20989] [PMID: 18381624]
[98]
Pappalardo JS, Quattrocchi V, Langellotti C, et al. Improved transfection of spleen-derived antigen-presenting cells in culture using TATp-liposomes. J Control Release 2009; 134(1): 41-6.
[http://dx.doi.org/10.1016/j.jconrel.2008.11.006] [PMID: 19059290]
[99]
Liu J, Zhang Q, Remsen EE, Wooley KL. Nanostructured materials designed for cell binding and transduction. Biomacromolecules 2001; 2(2): 362-8.
[http://dx.doi.org/10.1021/bm015515c] [PMID: 11749193]
[100]
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.
[http://dx.doi.org/10.1073/pnas.151247498] [PMID: 11438707]
[101]
Mattern-Schain SI, Fisher RK, West PC, et al. Cell mimetic liposomal nanocarriers for tailored delivery of vascular therapeutics. Chem Phys Lipids 2019; 218: 149-57.
[http://dx.doi.org/10.1016/j.chemphyslip.2018.12.009] [PMID: 30582896]
[102]
Nakamura T, Moriguchi R, Kogure K, Shastri N, Harashima H. Efficient MHC class I presentation by controlled intracellular trafficking of antigens in octaarginine-modified liposomes. Mol Ther 2008; 16(8): 1507-14.
[http://dx.doi.org/10.1038/mt.2008.122] [PMID: 18560420]
[103]
Nakamura T, Ono K, Suzuki Y, Moriguchi R, Kogure K, Harashima H. Octaarginine-modified liposomes enhance cross-presentation by promoting the C-terminal trimming of antigen peptide. Mol Pharm 2014; 11(8): 2787-95.
[http://dx.doi.org/10.1021/mp500147y] [PMID: 24901376]
[104]
Lim M, Badruddoza AZM, Firdous J, et al. Engineered nanodelivery systems to improve DNA vaccine technologies. Pharmaceutics 2020; 12(1): 1-29.
[http://dx.doi.org/10.3390/pharmaceutics12010030] [PMID: 31906277]
[105]
Hong SJ, Ahn MH, Lee YW, et al. Biodegradable polymeric nanocarrier-Based immunotherapy in hepatitis vaccination in cutting-edge enabling technologies for regenerative medicine. Berlin, Germany: Springer 2018; pp. 303-20.
[http://dx.doi.org/10.1007/978-981-13-0950-2_16]
[106]
Shae D, Postma A, Wilson JT. Vaccine delivery: Where polymer chemistry meets immunology. Future Sci 2016; 7.
[107]
Shen C, Li J, Zhang Y, et al. Polyethylenimine-based micro/nanoparticles as vaccine adjuvants. Int J Nanomedicine 2017; 12: 5443-60.
[http://dx.doi.org/10.2147/IJN.S137980] [PMID: 28814862]
[108]
Torchilin VP. Tatp-mediated intracellular delivery of pharmaceutical nanocarriers. Biochem Soc Trans 2007; 35(Pt 4): 816-20.
[http://dx.doi.org/10.1042/BST0350816] [PMID: 17635155]
[109]
Shahbazi R, Asik E, Kahraman N, Turk M, Ozpolat B, Ulubayram K. Modified gold-based siRNA nanotherapeutics for targeted therapy of triple-negative breast cancer. Nanomedicine (Lond) 2017; 12(16): 1961-73.
[http://dx.doi.org/10.2217/nnm-2017-0081] [PMID: 28745127]
[110]
Niu J, Chu Y, Huang YF, et al. Transdermal gene delivery by functional peptide-conjugated cationic gold nanoparticle reverses the progression and metastasis of cutaneous melanoma. ACS Appl Mater Interfaces 2017; 9(11): 9388-401.
[http://dx.doi.org/10.1021/acsami.6b16378] [PMID: 28252938]
[111]
Chereddy KK, Vandermeulen G, Préat V. PLGA based drug delivery systems: Promising carriers for wound healing activity. Wound Repair Regen 2016; 24(2): 223-36.
[http://dx.doi.org/10.1111/wrr.12404] [PMID: 26749322]
[112]
Liu SY, Wei W, Yue H, et al. Nanoparticles-based multi-adjuvant whole cell tumor vaccine for cancer immunotherapy. Biomaterials 2013; 34(33): 8291-300.
[http://dx.doi.org/10.1016/j.biomaterials.2013.07.020] [PMID: 23910466]
[113]
Liu X, Liu J, Liu D, et al. A cell-penetrating peptide-assisted nanovaccine promotes antigen cross-presentation and anti-tumor immune response. Biomater Sci 2019; 7(12): 5516-27.
[http://dx.doi.org/10.1039/C9BM01183H] [PMID: 31670734]
[114]
Coolen AL, Lacroix C, Mercier-Gouy P, et al. Poly(lactic acid) nanoparticles and cell-penetrating peptide potentiate mRNA-based vaccine expression in dendritic cells triggering their activation. Biomaterials 2019; 195: 23-37.
[http://dx.doi.org/10.1016/j.biomaterials.2018.12.019] [PMID: 30610991]
[115]
Zhang N, Chen H, Liu AY, et al. Gold conjugate-based liposomes with hybrid cluster bomb structure for liver cancer therapy. Biomaterials 2016; 74: 280-91.
[http://dx.doi.org/10.1016/j.biomaterials.2015.10.004] [PMID: 26461120]
[116]
Pack DW, Hoffman AS, Pun S, Stayton PS. Design and development of polymers for gene delivery. Nat Rev Drug Discov 2005; 4(7): 581-93.
[http://dx.doi.org/10.1038/nrd1775] [PMID: 16052241]
[117]
Malhotra M, Tomaro-Duchesneau C, Saha S, Prakash S. siRNA delivery to the brain by TAT/MGF tagged PEGylated chitosan nanoparticles. J Pharm (Cairo) 2013; 2013: 812387.
[http://dx.doi.org/10.1155/2013/812387] [PMID: 26555995]
[118]
Wang CQ, Wu JL, Zhuo RX, Cheng SX. Protamine sulfate-calcium carbonate-plasmid DNA ternary nanoparticles for efficient gene delivery. Mol Biosyst 2014; 10(3): 672-8.
[http://dx.doi.org/10.1039/c3mb70502a] [PMID: 24442276]
[119]
Wang K, Yang Y, Xue W, Liu Z. Cell Penetrating peptide-based redox-sensitive vaccine delivery system for subcutaneous vaccination. Mol Pharm 2018; 15(3): 975-84.
[http://dx.doi.org/10.1021/acs.molpharmaceut.7b00905] [PMID: 29359945]
[120]
Ryoo SR, Jang H, Kim KS, et al. Functional delivery of DNAzyme with iron oxide nanoparticles for hepatitis C virus gene knockdown. Biomaterials 2012; 33(9): 2754-61.
[http://dx.doi.org/10.1016/j.biomaterials.2011.12.015] [PMID: 22206595]
[121]
Wang ZY, Zhao Y, Ren L, et al. Novel gelatin-siloxane nanoparticles decorated by Tat peptide as vectors for gene therapy. Nanotechnology 2008; 19(44): 445103.
[http://dx.doi.org/10.1088/0957-4484/19/44/445103] [PMID: 21832720]
[122]
Shen Y, Qiu L. Effective oral delivery of gp100 plasmid vaccine against metastatic melanoma through multi-faceted blending-by-blending nanogels. Nanomedicine (Lond) 2019; 22: 102114.
[http://dx.doi.org/10.1016/j.nano.2019.102114] [PMID: 31655203]
[123]
Sakuma S, Suita M, Inoue S, et al. Cell-penetrating peptide-linked polymers as carriers for mucosal vaccine delivery. Mol Pharm 2012; 9(10): 2933-41.
[http://dx.doi.org/10.1021/mp300329r] [PMID: 22953762]
[124]
Gwak SJ, Nice J, Zhang J, et al. Cationic, amphiphilic copolymer micelles as nucleic acid carriers for enhanced transfection in rat spinal cord. Acta Biomater 2016; 35: 98-108.
[http://dx.doi.org/10.1016/j.actbio.2016.02.013] [PMID: 26873365]
[125]
Kanazawa T, Akiyama F, Kakizaki S, Takashima Y, Seta Y. Delivery of siRNA to the brain using a combination of nose-to-brain delivery and cell-penetrating peptide-modified nano-micelles. Biomaterials 2013; 34(36): 9220-6.
[http://dx.doi.org/10.1016/j.biomaterials.2013.08.036] [PMID: 23992922]
[126]
Kanazawa T, Kurano Y, Ibaraki H, et al. Therapeutic effects in a transient middle cerebral artery occlusion rat model by nose-to-brain delivery of anti-TNF-alpha siRNA with cell-penetrating peptide-modified polymer micelles. Pharmaceutics 2019; 11: 478.
[http://dx.doi.org/10.3390/pharmaceutics11090478]
[127]
Becker ML, Bailey LO, Wooley KL. Peptide-derivatized shell-cross-linked nanoparticles. 2. Biocompatibility evaluation. Bioconjug Chem 2004; 15(4): 710-7.
[http://dx.doi.org/10.1021/bc049945m] [PMID: 15264857]
[128]
Zope H, Quer CB, Bomans PH, Sommerdijk NA, Kros A, Jiskoot W. Peptide amphiphile nanoparticles enhance the immune response against a CpG-adjuvanted influenza antigen. Adv Healthc Mater 2014; 3(3): 343-8.
[http://dx.doi.org/10.1002/adhm.201300247] [PMID: 23983195]
[129]
Choi SW, Lee SH, Mok H, Park TG. Multifunctional siRNA delivery system: polyelectrolyte complex micelles of six-arm PEG conjugate of siRNA and cell penetrating peptide with crosslinked fusogenic peptide. Biotechnol Prog 2010; 26(1): 57-63.
[PMID: 19918765]
[130]
Rádis-Baptista G, Campelo IS, Morlighem JRL, Melo LM, Freitas VJF. Cell-penetrating peptides (CPPs): From delivery of nucleic acids and antigens to transduction of engineered nucleases for application in transgenesis. J Biotechnol 2017; 252: 15-26.
[http://dx.doi.org/10.1016/j.jbiotec.2017.05.002] [PMID: 28479163]
[131]
Olson ES, Aguilera TA, Jiang T, et al. In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer. Integr Biol 2009; 1(5-6): 382-93.
[http://dx.doi.org/10.1039/b904890a] [PMID: 20023745]
[132]
Bolton SJ, Jones DNC, Darker JG, Eggleston DS, Hunter AJ, Walsh FS. Cellular uptake and spread of the cell-permeable peptide penetratin in adult rat brain. Eur J Neurosci 2000; 12(8): 2847-55.
[http://dx.doi.org/10.1046/j.1460-9568.2000.00171.x] [PMID: 10971627]
[133]
Low W, Mortlock A, Petrovska L, Dottorini T, Dougan G, Crisanti A. Functional cell permeable motifs within medically relevant proteins. J Biotechnol 2007; 129(3): 555-64.
[http://dx.doi.org/10.1016/j.jbiotec.2007.01.019] [PMID: 17331607]

Rights & Permissions Print Cite
Article Metrics
82
1
World Malaria Day
© 2024 Bentham Science Publishers | Privacy Policy