Generic placeholder image

Current Drug Delivery

Editor-in-Chief

ISSN (Print): 1567-2018
ISSN (Online): 1875-5704

Review Article

Cell-penetrating Peptides: Efficient Vectors for Vaccine Delivery

Author(s): Jieru Yang, Yacheng Luo, Mohini Anjna Shibu, Istvan Toth* and Mariusz Skwarczynskia*

Volume 16, Issue 5, 2019

Page: [430 - 443] Pages: 14

DOI: 10.2174/1567201816666190123120915

Abstract

Subunit vaccines are composed of pathogen fragments that, on their own, are generally poorly immunogenic. Therefore, the incorporation of an immunostimulating agent, e.g. adjuvant, into vaccine formulation is required. However, there are only a limited number of licenced adjuvants and their immunostimulating ability is often limited, while their toxicity can be substantial. To overcome these problems, a variety of vaccine delivery systems have been proposed. Most of them are designed to improve the stability of antigen in vivo and its delivery into immune cells. Cell-penetrating peptides (CPPs) are especially attractive component of antigen delivery systems as they have been widely used to enhance drug transport into the cells. Fusing or co-delivery of antigen with CPPs can enhance antigen uptake, processing and presentation by antigen presenting cells (APCs), which are the fundamental steps in initiating an immune response. This review describes the different mechanisms of CPP intercellular uptake and various CPP-based vaccine delivery strategies.

Keywords: Cell-penetrating peptide, vaccine delivery, antigen presenting cells, adjuvant, antigen uptake, humoral and cellular immunity.

Graphical Abstract
[1]
Maurer, D.M.; Harrington, B.; Lane, J.M. Smallpox vaccine: Contraindications, administration, and adverse reactions. Am. Fam. Physician, 2003, 68, 889-906.
[2]
Lakhani, S. Early clinical pathologists: Edward Jenner (1749-1823). J. Clin. Pathol., 1992, 45, 756.
[3]
Alonso, P.L.; Tanner, M. Public health challenges and prospects for malaria control and elimination. Nat. Med., 2013, 19, 150.
[4]
Alm, J.S.; Lilja, G.; Pershagen, G.; Scheynius, A. Early BCG vaccination and development of atopy. Lancet, 1997, 350, 400-403.
[5]
Bull, J.J. Evolutionary reversion of live viral vaccines: Can genetic engineering subdue it? Virus Evol., 2015, 1, vev005.
[6]
Baxter, D. Active and passive immunity, vaccine types, excipients and licensing. Occup. Med. , 2007, 57, 552-556.
[7]
Koj, S.; Ługowski, C.; Niedziela, T. Bordetella pertussis lipooligosaccharide-derived neoglycoconjugates-new components of pertussis vaccine. Postepy Hig. Med. Dosw.(Online), 2015, 69, 1013-1030.
[8]
Singh, M.; O’Hagan, D. Advances in vaccine adjuvants. Nat. Biotechnol., 1999, 17, 1075.
[9]
Steer, A.C.; Law, I.; Matatolu, L.; Beall, B.W.; Carapetis, J.R. Global emm type distribution of group A streptococci: Systematic review and implications for vaccine development. Lancet Infect. Dis., 2009, 9, 611-616.
[10]
Skwarczynski, M.; Toth, I. Peptide-based synthetic vaccines. Chem. Sci. , 2016, 7, 842-854.
[11]
Jaberolansar, N.; Toth, I.; Young, P.R.; Skwarczynski, M. Recent advances in the development of subunit-based RSV vaccines. Expert Rev. Vaccines, 2016, 15, 53-68.
[12]
Skwarczynski, M.; Toth, I. Recent advances in peptide-based subunit nanovaccines. Nanomedicine, 2014, 9, 2657-2669.
[13]
Moyle, P.M.; Toth, I. Modern subunit vaccines: Development, components, and research opportunities. Chem. Med. Chem., 2013, 8, 360-376.
[14]
Nevagi, R.J.; Toth, I.; Skwarczynski, M. Peptide-based vaccines. In: Peptide Applications in Biomedicine, Biotechnology and Bioengineering; Koutsopoulos, S., Ed.; Woodhead Publishing: Cambridge, United Kingdom, 2018; pp. 327-358.
[15]
Azmi, F.; Ahmad Fuaad, A.A.; Skwarczynski, M.; Toth, I. Recent progress in adjuvant discovery for peptide-based subunit vaccines. Hum. Vaccin. Immunother., 2014, 10, 778-796.
[16]
Reed, S.G.; Orr, M.T.; Fox, C.B. Key roles of adjuvants in modern vaccines. Nat. Med., 2013, 19, 1597-1608.
[17]
Montomoli, E.; Piccirella, S.; Khadang, B.; Mennitto, E.; Camerini, R.; De Rosa, A. Current adjuvants and new perspectives in vaccine formulation. Expert Rev. Vaccines, 2011, 10, 1053-1061.
[18]
Zhao, G.; Chandrudu, S.; Skwarczynski, M.; Toth, I. The application of self-assembled nanostructures in peptide-based subunit vaccine development. Eur. Polym. J., 2017, 93, 670-681.
[19]
Hussein, W.M.; Liu, T.Y.; Skwarczynski, M.; Toth, I. Toll-like receptor agonists: A patent review (2011-2013). Expert Opin. Ther. Pat., 2014, 24, 453-470.
[20]
Deshayes, S.; Morris, M.C.; Divita, G.; Heitz, F. Cell-penetrating peptides: tools for intracellular delivery of therapeutics. Cell. Mol. Life Sci., 2005, 62, 1839-1849.
[21]
Chen, X. Current and future technological advances in transdermal gene delivery. Adv. Drug Deliv. Rev., 2018, 127, 85-105.
[22]
Rádis-Baptista, G.; Campelo, I.S.; Morlighem, J-É.R.; Melo, L.M.; Freitas, V.J. 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.
[23]
Chen, J.; Guan, X.; Hu, Y.; Tian, H.; Chen, X. Peptide-Based and Polypeptide-Based Gene Delivery Systems. Top. Curr. Chem. (Cham), 2017, 375, 32.
[24]
Lindgren, M.; Hällbrink, M.; Prochiantz, A.; Langel, Ü. Cell-penetrating peptides. Trends Pharmacol. Sci., 2000, 21, 99-103.
[25]
Green, M.; Loewenstein, P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell, 1988, 55, 1179-1188.
[26]
Frankel, A.D.; Pabo, C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 1988, 55, 1189-1193.
[27]
Wender, P.A.; Mitchell, D.J.; Pattabiraman, K.; Pelkey, E.T.; Steinman, L.; Rothbard, J.B. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc. Natl. Acad. Sci. USA, 2000, 97, 13003-13008.
[28]
Heitz, F.; Morris, M.C.; Divita, G. Twenty years of cell‐penetrating peptides: From molecular mechanisms to therapeutics. Br. J. Pharmacol., 2009, 157, 195-206.
[29]
Morris, M.; Vidal, P.; Chaloin, L.; Heitz, F.; Divita, G. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res., 1997, 25, 2730-2736.
[30]
Tünnemann, G.; Ter‐Avetisyan, G.; Martin, R.M.; Stöckl, M.; Herrmann, A.; Cardoso, M.C. Live‐cell analysis of cell penetration ability and toxicity of oligo‐arginines. J. Pept. Sci., 2008, 14, 469-476.
[31]
Derossi, D.; Joliot, A.H.; Chassaing, G.; Prochiantz, A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem., 1994, 269, 10444-10450.
[32]
Vives, E.; Brodin, P.; Lebleu, B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem., 1997, 272, 16010-16017.
[33]
Noguchi, H.; Matsushita, M.; Matsumoto, S.; Lu, Y-F.; Matsui, H.; Bonner-Weir, S. Mechanism of PDX-1 protein transduction. Biochem. Biophys. Res. Commun., 2005, 332, 68-74.
[34]
Bartlett, R.L.; Panitch, A. Thermosensitive nanoparticles with pH-triggered degradation and release of anti-inflammatory cell-penetrating peptides. Biomacromolecules, 2012, 13, 2578-2584.
[35]
Elliott, G.; O’Hare, P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell, 1997, 88, 223-233.
[36]
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 Biomembr., 1998, 1414, 127-139.
[37]
Morris, M.C.; 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, 1173.
[38]
Crombez, L.; Aldrian-Herrada, G.; Konate, K.; Nguyen, Q.N.; McMaster, G.K.; Brasseur, R.; Heitz, F.; Divita, G. A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells. Mol. Ther., 2009, 17, 95-103.
[39]
Nan, Y.H.; Park, I.S.; Hahm, K.S.; Shin, S.Y. Antimicrobial activity, bactericidal mechanism and LPS‐neutralizing activity of the cell‐penetrating peptide pVEC and its analogs. J. Pept. Sci., 2011, 17, 812-817.
[40]
Pooga, M.; Hällbrink, M.; Zorko, M. Cell penetration by transportan. FASEB J., 1998, 12, 67-77.
[41]
Rhee, M.; Davis, P. Mechanism of uptake of C105Y, a novel cell-penetrating peptide. J. Biol. Chem., 2006, 281, 1233-1240.
[42]
Gao, S.; Simon, M.J.; Hue, C.D.; Morrison, III, B.; Banta, S. An unusual cell penetrating peptide identified using a plasmid display-based functional selection platform. ACS Chem. Biol., 2011, 6, 484-491.
[43]
Peptides, C.P. Intracellular Pathways and Pharmaceutical Perspectives Patel, Leena N.; Zaro, Jennica L.; Shen, Wei-Chiang. Pharm. Res., 2007, 24, 1977-1992.
[44]
Duchardt, F.; Fotin‐Mleczek, M.; Schwarz, H.; Fischer, R.; Brock, R. A comprehensive model for the cellular uptake of cationic cell‐penetrating peptides. Traffic, 2007, 8, 848-866.
[45]
Fittipaldi, A.; Ferrari, A.; Zoppé, M.; Arcangeli, C.; Pellegrini, V.; Beltram, F.; Giacca, M. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem., 2003, 278, 34141-34149.
[46]
Tali, C. Scavenger receptors as a target for nucleic acid delivery with peptide vectors, Pooga, M; Padarik, K., Ed.; University of Tarita Press, 2017.
[47]
Madani, F.; Lindberg, S.; Langel, Ü.; Futaki, S.; Gräslund, A. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys., 2011, 2011, 414729.
[48]
Khandia, R.; Munjal, A.; Kumar, A.; Singh, G.; Karthik, K.; Dhama, K. Cell penetrating peptides: Biomedical/therapeutic applications with emphasis as promising futuristic hope for treating cancer. Int. J. Pharm., 2017, 13, 677-689.
[49]
Derossi, D.; Chassaing, G.; Prochiantz, A. Trojan peptides: The penetratin system for intracellular delivery. Trends Cell Biol., 1998, 8, 84-87.
[50]
Elmquist, A. Cell-penetrating peptides: Cellular uptake and biological activities; Stockholm University, 2003.
[51]
Pouny, Y.; Rapaport, D.; Mor, A.; Nicolas, P.; Shai, Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogs with phospholipid membranes. Biochemistry, 1992, 31, 12416-12423.
[52]
Wang, F.; Wang, Y.; Zhang, X.; Zhang, W.; Guo, S.; Jin, F. Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery. J. Control. Release, 2014, 174, 126-136.
[53]
Islam, M.Z.; Sharmin, S.; Moniruzzaman, M.; Yamazaki, M. Elementary processes for the entry of cell-penetrating peptides into lipid bilayer vesicles and bacterial cells. Appl. Microbiol. Biotechnol., 2018, 102, 3879-3892.
[54]
Futaki, S.; Nakase, I.; Tadokoro, A.; Takeuchi, T.; Jones, A.T. Arginine-rich peptides and their internalization mechanisms; In Portland Press Limited: England, United Kingdom, 2007.
[55]
Mousavi, S.A.; Malerød, L.; Trond, B.; Kjeken, R. Clathrin-dependent endocytosis. Biochem. J., 2004, 377, 1-16.
[56]
Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature, 2003, 422, 37.
[57]
Pujals, S.; Giralt, E. Proline-rich, amphipathic cell-penetrating peptides. Adv. Drug Deliv. Rev., 2008, 60, 473-484.
[58]
Futaki, S.; Nakase, I. Cell-surface interactions on arginine-rich cell-penetrating peptides allow for multiplex modes of internalization. Acc. Chem. Res., 2017, 50, 2449-2456.
[59]
El-Sayed, A.; Harashima, H. Endocytosis of gene delivery vectors: From clathrin-dependent to lipid raft-mediated endocytosis. Mol. Ther., 2013, 21, 1118-1130.
[60]
Aderem, A.; Underhill, D.M. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol., 1999, 17, 593-623.
[61]
Hillaireau, H.; Couvreur, P. Nanocarriers’ entry into the cell: Relevance to drug delivery. Cell. Mol. Life Sci., 2009, 66, 2873-2896.
[62]
Zaro, J.L.; Shen, W-C. Quantitative comparison of membrane transduction and endocytosis of oligopeptides. Biochem. Biophys. Res. Commun., 2003, 307, 241-247.
[63]
Futaki, S.; Suzuki, T.; Ohashi, W.; Yagami, T.; Tanaka, S.; Ueda, K.; Sugiura, Y. Arginine-rich peptides An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem., 2001, 276, 5836-5840.
[64]
Chaplin, D.D. Overview of the immune response. J. Allergy Clin. Immunol. Pract., 2010, 125, S3-S23.
[65]
Turvey, S.E.; Broide, D.H. Innate immunity. J. Allergy Clin. Immunol., 2010, 125, S24-S32.
[66]
Janeway, Jr, C.A.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol., 2002, 20, 197-216.
[67]
Janeway, Jr, C.A.; Travers, P.; Walport, M.; Shlomchik, M.J. The major histocompatibility complex and its functions; Garland Science: New York, USA, 2001.
[68]
Delves, P.J.; Martin, S.J.; Burton, D.R.; Roitt, I.M. Essential immunology; John Wiley & Sons: New Jersey, United States, 2017.
[69]
Bottomly, K. A functional dichotomy in CD4+ T lymphocytes. Immunol. Today, 1988, 9, 268-274.
[70]
Romagnani, S. Type 1 T helper and type 2 T helper cells: Functions, regulation and role in protection and disease. Int. J. Clin. Lab. Res., 1992, 21, 152-158.
[71]
Bonilla, F.A.; Oettgen, H.C. Adaptive immunity. J. Allergy Clin. Immunol. Pract., 2010, 125, S33-S40.
[72]
Saper, C.B. A guide to the perplexed on the specificity of antibodies. J. Histochem. Cytochem., 2009, 57, 1-5.
[73]
Borghesi, L.; Milcarek, C. From B cell to plasma cell. Immunol. Res., 2006, 36, 27-32.
[74]
Gulzar, N.; Copeland, K.F. CD8+ T-cells: Function and response to HIV infection. Curr. HIV Res., 2004, 2, 23-37.
[75]
Moticka, E.J. A historical perspective on evidence-based immunology; Newnes: Oxford, USA, 2015.
[76]
MacLeod, M.K.; Kappler, J.W.; Marrack, P. Memory CD4 T cells: Generation, reactivation and re‐assignment. Immunology, 2010, 130, 10-15.
[77]
Yu, Y-H.; Lin, K-I. Factors that regulate the generation of antibody-secreting plasma cells. In: Advances in immunology; Elsevier: Oxford, USA, 2016; Vol. 131, pp. 61-99.
[78]
Van Parijs, L.; Abbas, A.K. Homeostasis and self-tolerance in the immune system: Turning lymphocytes off. Science, 1998, 280, 243-248.
[79]
Trombetta, E.S.; Mellman, I. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol., 2005, 23, 975-1028.
[80]
Jiang, Y.; Li, M.; Zhang, Z.; Gong, T.; Sun, X. Cell-penetrating peptides as delivery enhancers for vaccine. Curr. Pharm. Biotechnol., 2014, 15, 256-266.
[81]
Zhang, Y.; Røise, J.J.; Lee, K.; Li, J.; Murthy, N. Recent developments in intracellular protein delivery. Curr. Opin. Biotechnol., 2018, 52, 25-31.
[82]
Sharfstein, S.T. Non-protein biologic therapeutics. Curr. Opin. Biotechnol., 2018, 53, 65-75.
[83]
Bahadoran, A.; Ebrahimi, M.; Yeap, S.K.; Safi, N.; Moeini, H.; Hair-Bejo, M.; Hussein, M.Z.; Omar, A.R. Induction of a robust immune response against avian influenza virus following transdermal inoculation with H5-DNA vaccine formulated in modified dendrimer-based delivery system in mouse model. Int. J. Nanomedicine, 2017, 12, 8573.
[84]
Ji, Z.; Xie, Z.; Zhang, Z.; Gong, T.; Sun, X. Engineering intravaginal vaccines to overcome mucosal and epithelial barriers. Biomaterials, 2017, 128, 8-18.
[85]
Tang, J.; Yin, R.; Tian, Y.; Huang, Z.; Shi, J.; Fu, X.; Wang, L.; Wu, Y.; Hao, F.; Ni, B. A novel self-assembled nanoparticle vaccine with HIV-1 Tat49-57/HPV16 E749-57 fusion peptide and GM-CSF DNA elicits potent and prolonged CD8+ T cell-dependent anti-tumor immunity in mice. Vaccine, 2012, 30, 1071-1082.
[86]
MuÈnger K.; Basile, J.R.; Duensing, S.; Eichten, A.; Gonzalez, S.L.; Grace, M.; Zacny, V.L. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene, 2001, 20, 7888.
[87]
Bonnem, E.M.; Chaudry, I.A.; Stupak, E. Use of GM-CSF as a vaccine adjuvant.In Google Patents: US5679356A, 1997.
[88]
Yang, Z.; Wang, L.; Wang, H.; Shang, X.; Niu, W.; Li, J.; Wu, Y. A novel mimovirus vaccine containing survivin epitope with adjuvant IL-15 induces long-lasting cellular immunity and high antitumor efficiency. Mol. Immunol., 2008, 45, 1674-1681.
[89]
Sun, Y.; Hu, Y-h. 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, 96-103.
[90]
Weinstein, M.R.; Litt, M.; Kertesz, D.A.; Wyper, P.; Rose, D.; Coulter, M.; McGeer, A.; Facklam, R.; Ostach, C.; Willey, B.M. Invasive infections due to a fish pathogen, Streptococcus iniae. N. Engl. J. Med., 1997, 337, 589-594.
[91]
Chen, X.; Lai, J.; Pan, Q.; Tang, Z.; Yu, Y.; Zang, G. The delivery of HBcAg via Tat-PTD enhances specific immune response and inhibits Hepatitis B virus replication in transgenic mice. Vaccine, 2010, 28, 3913-3919.
[92]
Zhang, Y.; Ning, J-F.; Qu, X-q.; Meng, X-L.; Xu, J-P. TAT-mediated oral subunit vaccine against white spot syndrome virus in crayfish. J. Virol. Methods, 2012, 181, 59-67.
[93]
Kronenberg, K.; Brosch, S.; Butsch, F.; Tada, Y.; Shibagaki, N.; Udey, M.C.; Von Stebut, E. Vaccination with TAT-antigen fusion protein induces protective, CD8+ T cell-mediated immunity against Leishmania major. J. Invest. Dermatol., 2010, 130, 2602-2610.
[94]
Dong, H.; Jing, W.; Yingru, X.; Wenyang, W.; Ru, C.; Shengfa, N.; Congjing, X.; Jingjing, D.; Wan, W.; Jiang, H. Enhanced anti-tuberculosis immunity by a TAT-Ag85B protein vaccine in a murine tuberculosis model. Pathog. Glob. Health, 2015, 109, 363-368.
[95]
Huang, H-C.; Lu, H-F.; Lai, Y-H.; Lee, C-P.; Liu, H-K.; Huang, C. Tat-enhanced delivery of the C terminus of HDAg-L inhibits assembly and secretion of hepatitis D virus. Antivir Res., 2018, 150, 69-78.
[96]
Sakuma, S.; Suita, M.; Inoue, S.; Marui, Y.; Nishida, K.; Masaoka, Y.; Kataoka, M.; Yamashita, S.; Nakajima, N.; Shinkai, N. Cell-penetrating peptide-linked polymers as carriers for mucosal vaccine delivery. Mol. Pharm., 2012, 9, 2933-2941.
[97]
Mohri, K.; Miyata, K.; Egawa, T.; Tanishita, S.; Endo, R.; Yagi, H.; Ukawa, M.; Ochiai, K.; Hiwatari, K-I.; Tsubaki, K. 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, 375-381.
[98]
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, 1507-1514.
[99]
Nakamura, T.; Yamazaki, D.; Yamauchi, J.; Harashima, H. The nanoparticulation by octaarginine-modified liposome improves α-galactosylceramide-mediated antitumor therapy via systemic administration. J. Control. Release, 2013, 171, 216-224.
[100]
Wang, K.; Yang, Y.; Xue, W.; Liu, Z. Cell penetrating peptide-based redox-sensitive vaccine delivery system for subcutaneous vaccination. Mol. Pharm., 2018, 15, 975-984.
[101]
Zhang, Y.; Li, H.; Wang, Q.; Hao, X.; Li, H.; Sun, H.; Han, L.; Zhang, Z.; Zou, Q.; Sun, X. Rationally designed self‐assembling nanoparticles to overcome mucus and epithelium transport barriers for oral vaccines against Helicobacter pylori. Adv. Funct. Mater., 2018, 28(33), 1802675.
[102]
Schutze-Redelmeier, M-P.M.; Kong, S.; Bally, M.B.; Dutz, J.P. Antennapedia transduction sequence promotes anti tumour immunity to epicutaneously administered CTL epitopes. Vaccine, 2004, 22, 1985-1991.
[103]
Pouniotis, D.S.; Esparon, S.; Apostolopoulos, V.; Pietersz, G.A. Whole protein and defined CD8+ and CD4+ peptides linked to penetratin targets both MHC class I and II antigen presentation pathways. Immunol. Cell Biol., 2011, 89, 904.
[104]
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, 2014-2017.
[105]
Brooks, N.; Hsu, J.; Esparon, S.; Pouniotis, D.; Pietersz, G. Immunogenicity of a tripartite cell penetrating peptide containing a MUC1 variable number of tandem repeat (VNTR) and AT helper epitope. Molecules, 2018, 23, 2233.
[106]
Taylor-Papadimitriou, J.; Burchell, J.M.; Graham, R.; Beatson, R. Latest developments in MUC1 immunotherapy. Biochem. Soc. Trans., 2018, 46, 659-668.
[107]
Elliott, G.; O’Hare, P. Intercellular trafficking of VP22-GFP fusion proteins. Gene Ther., 1999, 6, 149.
[108]
Hung, C-F.; Cheng, W-F.; Chai, C-Y.; Hsu, K-F.; He, L.; Ling, M.; Wu, T-C. Improving vaccine potency through intercellular spreading and enhanced MHC class I presentation of antigen. J. Immunol., 2001, 166, 5733-5740.
[109]
Cheng, W-F.; Hung, C-F.; Hsu, K-F.; Chai, C-Y.; He, L.; Polo, J.M.; Slater, L.A.; Ling, M.; Wu, T-C. Cancer immunotherapy using Sindbis virus replicon particles encoding a VP22–antigen fusion. Hum. Gene Ther., 2002, 13, 553-568.
[110]
Kim, T.W.; Hung, C-F.; Kim, J.W.; Juang, J.; Chen, P-J.; He, L.; Boyd, D.A.; Wu, T-C. Vaccination with a DNA vaccine encoding herpes simplex virus type 1 VP22 linked to antigen generates long-term antigen-specific CD8-positive memory T cells and protective immunity. Hum. Gene Ther., 2004, 15, 167-177.
[111]
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, 4399-4405.
[112]
Zheng, C.; Babiuk, L.A. Bovine herpesvirus 1 VP22 enhances the efficacy of a DNA vaccine in cattle. J. Virol., 2005, 79, 1948-1953.
[113]
Zheng, C.; Brownlie, R.; Huang, D.; Babiuk, L. Intercellular trafficking of the major tegument protein VP22 of bovine herpesvirus-1 and its application to improve a DNA vaccine. Arch. Virol., 2006, 151, 985-993.
[114]
Zhao, W.; Xiao, S-B.; Fang, L-R.; Jiang, Y.; Song, Y.; Yan, L.; Yu, X.; Chen, H. Immunogenicity of DNA vaccine expressing GP5 of porcine reproductive and respiratory syndrome virus fused with VP22 of bovine herpesvirus 1. Sheng Wu Gong Cheng Xue Bao Chin. J. Biotechnol., 2005, 21, 725-730.
[115]
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, 459-467.
[116]
Saleh, T.; Bolhassani, A.; Shojaosadati, S.A.; Aghasadeghi, M.R. MPG-based nanoparticle: An efficient delivery system for enhancing the potency of DNA vaccine expressing HPV16E7. Vaccine, 2015, 33, 3164-3170.

© 2024 Bentham Science Publishers | Privacy Policy