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Phage Particles as Vaccine Delivery Vehicles: Concepts, Applications and Prospects

  • Jafari, Narjes (Cellular and Molecular Biology, Immunogenetics Research Center, Faculty of Medicine, Mazandaran University of Medical Sciences) ;
  • Abediankenari, Saeid (Immunogenetics Research Center, Faculty of Medicine, Mazandaran University of Medical Sciences)
  • Published : 2016.01.11

Abstract

The development of new strategies for vaccine delivery for generating protective and long-lasting immune responses has become an expanding field of research. In the last years, it has been recognized that bacteriophages have several potential applications in the biotechnology and medical fields because of their intrinsic advantages, such as ease of manipulation and large-scale production. Over the past two decades, bacteriophages have gained special attention as vehicles for protein/peptide or DNA vaccine delivery. In fact, whole phage particles are used as vaccine delivery vehicles to achieve the aim of enhanced immunization. In this strategy, the carried vaccine is protected from environmental damage by phage particles. In this review, phage-based vaccine categories and their development are presented in detail, with discussion of the potential of phage-based vaccines for protection against microbial diseases and cancer treatment. Also reviewed are some recent advances in the field of phagebased vaccines.

Keywords

Bacteriophage;vaccine;carrier;immune response

References

  1. Abediankenari S, Ghasemi M, Nasehi MM, Abedi S, Hosseini V (2011). Determination of trace elements in patients with chronic Hepatitis B. Acta Medica Iranica, 49, 667-669.
  2. Abediankenari S, Janbabaei Mollae G, Ghasemi M, et al (2013).Vaccination of diffuse large B-cell lymphoma patients with antigen-primed dendritic cells. Acta Medica Iranica, 51, 284-288.
  3. Abediankenari S, Yousefzadeh Y, Azadeh H, Vahedi M (2010). Comparision of several maturation inducing factors indendritic cell differentiation. Iran J Immunol, 7, 83-87.
  4. Arap MA (2005). Phage display technology - Applications and innovations. Genet Mol Biol, 1, 1-9.
  5. Bahadir AO, Balcioglu BK, Uzyol KS, et al (2011). Phagedisplayed HBV core antigen with immunogenic activity. Appl Biochem Biotechnol, 165, 1437-47. https://doi.org/10.1007/s12010-011-9365-1
  6. Bakhshinejad B, Sadeghizadeh M (2014). Bacteriophages asvehicles for gene delivery into mammalian cells: prospects and problems. Expert Opin Drug deliv, 11.
  7. Bazan J, Calkosi.ski I, Gamian A (2012). Phage display.Apowerful technique for immunotherapy. Hum Vaccin Immunother, 8, 1829-35. https://doi.org/10.4161/hv.21704
  8. Bratkovic T (2010). Progress in phage display: evolution of the technique and its applications. Cell Mol Life Sci, 67, 749-67. https://doi.org/10.1007/s00018-009-0192-2
  9. Bruttin A, Brussow H (2005). Human volunteers receivingEscherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother, 49, 2874-8. https://doi.org/10.1128/AAC.49.7.2874-2878.2005
  10. Clark JR, March JB (2004). Bacteriophage-mediated nucleic acidimmunization. FEMS Immunol Med Microbiol, 40, 21-26. https://doi.org/10.1016/S0928-8244(03)00344-4
  11. Clark JR, March JB (2006). Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol, 24, 212-8. https://doi.org/10.1016/j.tibtech.2006.03.003
  12. Cortese R, Felici F, Galfre G, et al (1994). Epitope discovery using peptide libraries displayed on phage. Trends Biotechnol, 12, 262-7. https://doi.org/10.1016/0167-7799(94)90137-6
  13. Cuesta A M, Suarez E, Larsen M, et al (2006). Enhancement of DNA vaccine potency through linkage of antigen tofilamentous bacteriophage coat protein III domain I. Immunology, 117, 502-6. https://doi.org/10.1111/j.1365-2567.2006.02325.x
  14. De Berardinis P, Sartorius R, Fanutti C, et al (2000). Phagedisplay of peptide epitopes from HIV-1 elicits strongcytolytic responses. Nat Biotechnol, 18, 873-6. https://doi.org/10.1038/78490
  15. de la Cruz VF, Lal AA, McCutchan TF (1988). Immumogenicityand epitope mapping of foreign sequences via genetically engineered filamentous phage. J Biol Chem, 263, 4318-22.
  16. Delmastro P, Meola A, Monaci P, Cortese R, Galfre G (1997). Immunogenicity of filamentous phage displaying peptide mimotopes after oral administration. Vaccine, 15, 1276-85. https://doi.org/10.1016/S0264-410X(97)00072-8
  17. Eguchi A, Akuta T, Okuyama H, et al (2001). Protein transductiondomain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem, 276, 26204-10. https://doi.org/10.1074/jbc.M010625200
  18. Fack F, Hugle-Dorr B, Song D, et al (1997). Epitope mapping by phage display: random versus gene-fragment libraries. J Immunol Methods, 206, 43-52. https://doi.org/10.1016/S0022-1759(97)00083-5
  19. Fang J, Wang G, Yang Q, et al (2005). The potential of phage display virions expressing malignant tumor specific antigen MAGE-A1 epitope in murine model. Vaccine, 23, 4860-6. https://doi.org/10.1016/j.vaccine.2005.05.024
  20. Gamage LNA, Ellis J, Hayes S, et al (2009). Immunogenicity of bacteriophage lambda particles displaying porcineCircovirus 2 (PCV2) capsid protein epitopes. Vaccine, 27,6595-604. https://doi.org/10.1016/j.vaccine.2009.08.019
  21. Gao J, Liu Z, Huang M, Li X, Wang Z (2011). T7 phagedisplaying latent membrane protein 1 of Epstein-Barr virus elicits humoral and cellular immune responses in rats. Acta Virol, 55, 117-21. https://doi.org/10.4149/av_2011_02_117
  22. Gao J, Wang Y, Liu Z. Wang Z (2010). Phage display and its application in vaccine design. Ann Microbiol, 60, 13-19. https://doi.org/10.1007/s13213-009-0014-7
  23. Gaubin M, Fanutti C, Mishal Z, et al (2003). Processing offilamentous bacteriophage virions in antigen-presentingcells targets both HLA class I and class II peptide loading compartments. DNA Cell Biol, 22, 11-18. https://doi.org/10.1089/104454903321112451
  24. Ghaemi A, Soleimanjehi H, Gill P, et al (2010). Recombinant $\lambda$-phage nanobioparticles for tumor therapy in mice models. Genet Vaccines Ther, 8(3).
  25. Hashemi H, Pouyanfard S, Bandehpour M, et al (2012).Immunization with M2e-displaying T7 bacteriophagenanoparticles protects against influenza A virus vhallenge. PLOS ONE, 7, 1-11.
  26. Hayes S, Gamage NA, Hayes C (2010). Dual expression systemfor assembling phage lambda display particle (LDP) vaccineto porcine Circovirus 2 (PCV2). Vaccine, 28, 6789-99. https://doi.org/10.1016/j.vaccine.2010.07.047
  27. Irving MB, Pan O, Scott JK (2001). Random-peptide libraries and antigen-fragment libraries for epitope mapping and the development of vaccines and diagnostics. Curr Opin Chem Biol, 5, 314-24. https://doi.org/10.1016/S1367-5931(00)00208-8
  28. Ivanenkov VV, Felici F, Menon AG (1999). Uptake andintracellular fate of phage display vectors in mammalian cells. Biochim et Biophys Acta, 1448, 450-62. https://doi.org/10.1016/S0167-4889(98)00162-1
  29. Jepson CD, March JB (2004). Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine, 22, 2413-19. https://doi.org/10.1016/j.vaccine.2003.11.065
  30. Jiang J, Abu-Shilbayeh L, Rao BV (1997). Display of a PorApeptide from Neisseria meningitidis on the bacteriophage T4 capsid surface. Infect Immun, 65, 4770-77.
  31. Kaur T, Nafissi N, Wasfi O, et al (2012). Immunocompatibility of Bacteriophages as Nanomedicines. J Nanotechnol, 1-13.
  32. Khalaj-Kondori M, Sadeghizadeh M, Behmanesh M, Saggio I, Monaci P (2011). Chemical coupling as a potent strategy for preparation of targeted bacteriophage-derived genenanocarriers into eukaryotic cells. J Gene Med, 13, 622-31. https://doi.org/10.1002/jgm.1617
  33. Kim A, Shin TH, Shin SM, et al (2012). Cellular internalization mechanism and intracellular trafficking of filamentous M13phages displaying a cell penetrating transbody and TATpeptide. PLOS ONE, 7, 1-14.
  34. Knittelfelder R, Riemer AB, Jensen-Jarolim E, (2009). Mimotope vaccination . from allergy to cancer. Expert Opin Biol Ther, 9, 493-506. https://doi.org/10.1517/14712590902870386
  35. Koivunen E, Arap W, Rajotte D, Lahdenranta J, Pasqualini R (1999). Identification of receptor ligands with phage displaypeptide libraries. J Nucl Med, 40, 883-8.
  36. Lankes HA, Zanghi CN, Santos K, et al (2007). In vivo gene delivery and expression by bacteriophage lambda vectors. J Appl Microbiol, 102, 1337-49. https://doi.org/10.1111/j.1365-2672.2006.03182.x
  37. Li W, Joshi MD, Singhania S, Ramsey KH, Murthy AK (2014). Peptide vaccine: progress and challenges. Vaccines, 2,515-36. https://doi.org/10.3390/vaccines2030515
  38. Loessner MJ, Rudolf M, Scherer S (1997). Evaluation ofluciferase reporter bacteriophage A511::luxAB for detectionof Listeria monocytogenes in contaminated foods. Appl Environ Microbiol, 63, 2961-5.
  39. Luzzago A, Felici F, Tramontano A, Pessi A, Cortese R (1993). Mimicking of discontinuous epitopes by phage-displayed peptides, I. Epitope mapping of human H ferritin using a phage library of constrained peptides. Gene, 128, 51-57. https://doi.org/10.1016/0378-1119(93)90152-S
  40. Malik P, Perham RN (1997). Simultaneous display of different peptides on the surface of filamentous bacteriophage. Nucleic Acids Res, 25, 915-6. https://doi.org/10.1093/nar/25.4.915
  41. Manoutcharian K, Diaz-Orea A, Gevorkian G, et al (2004).Recombinant bacteriophage-based multiepitope vaccineagainst Taenia solium pig cysticercosis. Vet Immunol Immunopathol, 99, 11-24. https://doi.org/10.1016/j.vetimm.2003.12.009
  42. Manoutcharian K, Terrazas LI, Gevorkian G, et al (1999). Phage-displayed T-cell epitope grafted into immunoglobulin heavy-chain complementarity-determining regions: an effectivevaccine design tested in murine cysticercosis. Infect Immun, 67, 4764-4770.
  43. March JB, Clark JR, Jepson CD (2004). Genetic immunization against hepatitis B using whole bacteriophage $\lambda$ particles. Vaccine, 22, 1666-71. https://doi.org/10.1016/j.vaccine.2003.10.047
  44. Meij P, Leen A, Rickinson AB, et al (2002a). Identification and prevalence of CD8+ T-cell responses directed against Epstein-Bar virus-encoded latent membrane protein 1 and latent membrane protein 2. Int J Cancer, 99, 93-99. https://doi.org/10.1002/ijc.10309
  45. Meij P, Vervoort MBHJ, Bloemena E, et al (2002b). Antibody responses to Epstein-Barr virus-encoded latent membrane protein-1 (LMP1) and expression of LMP1 in juvenile Hodgkin's disease. J Med Virol, 68, 370-377. https://doi.org/10.1002/jmv.10213
  46. Menendez T, Santiago-Vispo NF, Cruz-Leal Y, et al (2011).Identification and characterization of phage-displayedpeptide mimetics of Neisseria meningitidis serogroup B capsular polysaccharide. Int J Med Microbiol, 301, 16-25. https://doi.org/10.1016/j.ijmm.2010.04.020
  47. Moingeon P, de Taisne C, Almond J (2002). Delivery technologies for human vaccines. Br Med Bull, 62, 29-44. https://doi.org/10.1093/bmb/62.1.29
  48. Neufeld T, Schwartz-Mittelmann A, Biran D, Ron EZ, Rishpon J(2003). Combined phage typing and amperometric detection of released enzymatic activity for the specific identification and quantification of bacteria. Anal Chem, 75, 580-5. https://doi.org/10.1021/ac026083e
  49. Odermatt A, Audige A, Frick C, et al (2001). Identification of receptor ligands by screening phage display peptide librariesex vivo on microdissected kidney tubules. J Am Soc Nephrol, 12, 308-16.
  50. Ou C, Tian D, Ling Y, et al (2013). Evaluation of an ompA-based phage-mediated DNA vaccine against Chlamydia abortusin piglets. Int immunopharmacol, 16, 505-10. https://doi.org/10.1016/j.intimp.2013.04.027
  51. Pande J, Szewczyk MM, Grover, AK (2010). Phage display: Concept, innovations, applications and future. Biotechnol Adv, 28, 849-58. https://doi.org/10.1016/j.biotechadv.2010.07.004
  52. Petrovsky N, Aguilar JC (2004). Vaccine adjuvants: Current stateand future trends. Immunol cell Biol, 82, 488-96. https://doi.org/10.1111/j.0818-9641.2004.01272.x
  53. Purcell AW, McCluskey J, Rossjohn J (2007). More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Disc, 6, 404-414. https://doi.org/10.1038/nrd2224
  54. Ren SX, Ren ZJ, Zhao MY, et al (2009). Antitumor activity of endogenous mFlt4 displayed on a T4 phage nanoparticle surface. Acta Pharmacol Sin, 30, 637-45. https://doi.org/10.1038/aps.2009.44
  55. Sartorius R, Pisu P, Apice LD, et al (2008). The use of filamentous bacteriophage fd to deliver MAGE-A10 or MAGE-A3 HLA­A2-restricted peptides and to induce strong antitumor CTL responses. J Immunol, 180, 3719-28. https://doi.org/10.4049/jimmunol.180.6.3719
  56. Saxena MV, M, Van TTH, Baird FJ, Coloe PJ, Smooker PM (2013). Pre-existing immunity against vaccine vectors -friend or foe? Microbiol, 159, 1-11. https://doi.org/10.1099/mic.0.049601-0
  57. Schmelcher M, Loessner MJ (2014). Application of bacteriophages for detection of foodborne pathogens. Bacteriophage, 4.
  58. Smith G P (1985). Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science, 228, 1315-7. https://doi.org/10.1126/science.4001944
  59. Souza APD, Haut L, Reyes-Sandoval A, Pinto, AR (2005). Recombinant viruses as vaccines against viral diseases. Brazi J Med Biol Res, 38, 509-22. https://doi.org/10.1590/S0100-879X2005000400004
  60. Ulivieri C, Citro A, Ivaldi F, et al (2008). Antigenic properties of HCMV peptides displayed by filamentous bacteriophagesvs. synthetic peptides. Immunol Lett, 119, 62-70. https://doi.org/10.1016/j.imlet.2008.04.004
  61. van Houten NE, Henry KA, Smith GP, Scott JK (2010).Engineering filamentous phage carriers to improve focusingof antibody responses against peptides. Vaccine, 28, 2174-­2185. https://doi.org/10.1016/j.vaccine.2009.12.059
  62. van Houten NE, Zwick MB, Menendez A, Scott JK (2006). Filamentous phage as an immunogenic carrier to elicitfocused antibody responses against a synthetic peptide.Vaccine, 24, 4188-200. https://doi.org/10.1016/j.vaccine.2006.01.001
  63. Wan Y, Yuzhang Y, Bian J, et al (2001). Induction of hepatitis B virus-specific cytotoxic T lymphocytes response in vivo by filamentous phage display vaccine. Vaccine, 19, 2918-23. https://doi.org/10.1016/S0264-410X(00)00561-2
  64. Wan Y, Wu Y, Zhou J, et al (2005). Cross-presentation of phage particle antigen in MHC class II and endoplasmic reticulum marker-positive compartments. Eur J Immunol, 35, 2041-50. https://doi.org/10.1002/eji.200425322
  65. Wang G, Sun M, Fang J, et al (2006). Protective immuneresponses against systemic candidiasis mediated by phage-displayed specific epitope of Candida albicans heat shock protein 90 in C57BL/6J mice. Vaccine, 24, 6065-6073. https://doi.org/10.1016/j.vaccine.2006.05.022
  66. Wang LF, Yu M (2004). Epitope identification and discovery using phage display libraries: applications in vaccine development and diagnostics. Curr Drug Targets, 5, 1-15.
  67. Wang Y, Su Q, Dong S, et al (2014). Hybrid phage displaying SLAQVKYTSASSI induces protection against Candidaalbicans challenge in BALB/c mice. Hum Vaccin Immunother, 10, 1057-63. https://doi.org/10.4161/hv.27714
  68. Willis AE, Perham RN, Wraith D (1993). Immunological properties of foreign peptides in multiple display on afilamentous bacteriophage. Gene, 128, 79-83. https://doi.org/10.1016/0378-1119(93)90156-W
  69. Winter G, Griffiths AD, Hawkins RE, Hoogenboom HR (1994). Making antibodies by phage display technology. Annu Rev Immunol, 12, 433-55. https://doi.org/10.1146/annurev.iy.12.040194.002245
  70. Wright A, Hawkins CH, Anggard EE, Harper DR (2009). A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin Otolaryngol, 34, 349-57. https://doi.org/10.1111/j.1749-4486.2009.01973.x
  71. Wu Y, Wan Y, Bian J, et al (2002). Phage display particles expressing tumor-specific antigens induce preventive and therapeutic anti-tumor immunity in murine P815 model. Int J Cancer, 98, 748-53. https://doi.org/10.1002/ijc.10260
  72. Yang J, Li Y, Jin S, et al (2015). Engineered biomaterials for development of nucleic acid vaccines. Biomater Res, 19.
  73. Yokoyama-Kobayashi M, Kato S (1994). Recombinant f1 phage-mediated transfection of mammalian cells using lipopolyamine technique. Anal Biochem, 223, 130-134. https://doi.org/10.1006/abio.1994.1557

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