Filamentous Bacteriophage for Immunotherapeutic Strategies: Comparison
Please note this is a comparison between Version 2 by Vivi Li and Version 1 by Rossella Sartorius.

The pharmaceutical use of bacteriophages as safe and inexpensive therapeutic tools is collecting renewed interest. The use of lytic phages to fight antibiotic-resistant bacterial strains is pursued in academic and industrial projects and is the object of several clinical trials. On the other hand, filamentous bacteriophages used for the phage display technology can also have diagnostic and therapeutic applications. Filamentous bacteriophages are nature-made nanoparticles useful for their size, the capability to enter blood vessels, and the capacity of high-density antigen expression. In the last decades, filamentous bacteriophage ‘fd’ was employed as antigen delivery system, able to trigger all arms of the immune response, with particular emphasis on the ability of the MHC class I restricted antigenic determinants displayed on phages to induce strong and protective cytotoxic responses.Moreover, fd bacteriophages, engineered to target mouse dendritic cells (DCs), activate innate and adaptive responses without the need of exogenous adjuvants, and more recently was employed for the display of immunologically active lipids.

  • filamentous bacteriophage
  • vaccine
  • nanoparticle
  • targeting
  • phage display
  • antigen delivery
Please wait, diff process is still running!

References

  1. Reardon, S. Phage therapy gets revitalized. Nature 2014, 510, 15–16.
  2. Schmidt, C. Phage therapy’s latest makeover. Nat. Biotechnol. 2019, 37, 581–586.
  3. Dedrick, R.M.; Guerrero-Bustamante, C.A.; Garlena, R.A.; Russell, D.A.; Ford, K.; Harris, K.; Gilmour, K.C.; Soothill, J.; Jacobs-Sera, D.; Schooley, R.T.; et al. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat. Med. 2019, 25, 730–733.
  4. Prisco, A.; De Berardinis, P. Filamentous Bacteriophage Fd as an Antigen Delivery System in Vaccination. Int. J. Mol. Sci. 2012, 13, 5179–5194.
  5. Hassapis, K.A.; Stylianou, D.C.; Kostrikis, L.G. Architectural Insight into Inovirus-Associated Vectors (IAVs) and Development of IAV-Based Vaccines Inducing Humoral and Cellular Responses: Implications in HIV-1 Vaccines. Viruses 2014, 6, 5047–5076.
  6. Sartorius, R.; Russo, D.; D’Apice, L.; De Berardinis, P.; Berardinis, P. Filamentous Bacteriophages: An Antigen and Gene Delivery System. In Innovation in Vaccinology; Springer Science and Business Media LLC: Berlin/Heidelberg, Germany, 2012; pp. 123–134.
  7. Henry, K.A.; Arbabi-Ghahroudi, M.; Scott, J.K. Beyond phage display: Non-traditional applications of the filamentous bacteriophage as a vaccine carrier, therapeutic biologic, and bioconjugation scaffold. Front. Microbiol. 2015, 6, 755.
  8. Aghebati-Maleki, L.; Bakhshinejad, B.; Baradaran, B.; Motallebnezhad, M.; Aghebati-Maleki, A.; Nickho, H.; Yousefi, M.; Majidi, J. Phage display as a promising approach for vaccine development. J. Biomed. Sci. 2016, 23, 66.
  9. Potocnakova, L.; Bhide, M.; Pulzova, L.B. An Introduction to B-Cell Epitope Mapping and In Silico Epitope Prediction. J. Immunol. Res. 2016, 2016, 6760830.
  10. Wang, L.F.; Yu, M. Epitope Identification and Discovery Using Phage Display Libraries: Applications in Vaccine Development and Diagnostics. Curr. Drug Targets 2004, 5, 1–15.
  11. Villa-Mancera, A.; Reynoso-Palomar, A.; Utrera-Quintana, F.; Carreon-Luna, L. Cathepsin L1 mimotopes with adjuvant quil a induces a th1/th2 immune response and confers significant protection against fasciola hepatica infection in goats. Parasitol. Res. 2014, 113, 243–250.
  12. Schiavone, M.; Fiume, G.; Caivano, A.; De Laurentiis, A.; Falcone, C.; Masci, F.F.; Iaccino, E.; Mimmi, S.; Palmieri, C.; Pisano, A.; et al. Design and Characterization of a Peptide Mimotope of the HIV-1 gp120 Bridging Sheet. Int. J. Mol. Sci. 2012, 13, 5674–5699.
  13. Xin, H.; Glee, P.; Adams, A.; Mohiuddin, F.; Eberle, K. Design of a mimotope-peptide based double epitope vaccine against disseminated candidiasis. Vaccine 2019, 37, 2430–2438.
  14. Mertens, P.; Walgraffe, D.; Laurent, T.; Deschrevel, N.; Letesson, J.J.; De Bolle, X. Selection of Phage-displayed Peptides Recognised by Monoclonal Antibodies Directed against the Lipopolysaccharide of Brucella. Int. Rev. Immunol. 2001, 20, 181–199.
  15. Khurana, S.; Suguitan, A.L.; Rivera, Y.; Simmons, C.P.; Lanzavecchia, A.; Sallusto, F.; Manischewitz, J.; King, L.R.; Subbarao, K.; Golding, H. Antigenic Fingerprinting of H5N1 Avian Influenza Using Convalescent Sera and Monoclonal Antibodies Reveals Potential Vaccine and Diagnostic Targets. PLoS Med. 2009, 6, e1000049.
  16. Khurana, S.; Chearwae, W.; Castellino, F.; Manischewitz, J.; King, L.R.; Honorkiewicz, A.; Rock, M.T.; Edwards, K.M.; Del Giudice, G.; Rappuoli, R.; et al. Vaccines with MF59 Adjuvant Expand the Antibody Repertoire to Target Protective Sites of Pandemic Avian H5N1 Influenza Virus. Sci. Transl. Med. 2010, 2.
  17. Ravichandran, S.; Hahn, M.; Belaunzarán-Zamudio, P.F.; Ramos-Castañeda, J.; Nájera-Cancino, G.; Caballero-Sosa, S.; Navarro-Fuentes, K.R.; Ruiz-Palacios, G.; Golding, H.; Beigel, J.H.; et al. Differential human antibody repertoires following Zika infection and the implications for serodiagnostics and disease outcome. Nat. Commun. 2019, 10, 1943.
  18. Luzar, J.; Štrukelj, B.; Lunder, M. Phage display peptide libraries in molecular allergology: From epitope mapping to mimotope based immunotherapy. Allergy 2016, 71, 1526–1532.
  19. Zahirović, A.; Lunder, M. Microbial Delivery Vehicles for Allergens and Allergen-Derived Peptides in Immunotherapy of Allergic Diseases. Front. Microbiol. 2018, 9, 1449.
  20. Jensen-Jarolim, E.; Leitner, A.; Kalchhauser, H.; Zürcher, A.; Ganglberger, E.; Bohle, B.; Scheiner, O.; Boltz-Nitulescu, G.; Breiteneder, H. Peptide mimotopes displayed by phage inhibit antibody binding to Bet v 1, the major birch pollen allergen, and induce specific IgG response in mice. FASEB J. 1998, 12, 1635–1642.
  21. Yang, Y.; Cao, M.J.; Alcocer, M.; Liu, Q.M.; Fei, D.X.; Mao, H.Y.; Liu, G.M. Mapping and characterization of antigenic epitopes of arginine kinase of Scylla paramamosain. Mol. Immunol. 2015, 65, 310–320.
  22. Tonelli, R.R.; Colli, W.; Alves, M.J. Selection of binding targets in parasites using phage-display and aptamer libraries in vivo and in vitro. Front. Immunol. 2012, 3, 419.
  23. Shi, H.; Dong, S.; Zhang, X.; Chen, X.; Gao, X.; Wang, L. Phage vaccines displaying YGKDVKDLFDYAQE epitope induce protection against systemic candidiasis in mouse model. Vaccine 2018, 36, 5717–5724.
  24. Wang, G.; Sun, M.; Fang, J.; Yang, Q.; Tong, H.; Wang, L. Protective immune responses against systemic candidiasis mediated by phage-displayed specific epitope of Candida albicans heat shock protein 90 in C57BL/6J mice. Vaccine 2006, 24, 6065–6073.
  25. Wang, Y.; Shi, H.; Dong, S.; Li, Y.; Wang, M.; Huai, Y.; Zhang, X.; Chen, X.; Mao, C.; Gao, X.; et al. Nontoxic engineered virus nanofibers as an efficient agent for the prevention and detection of fungal infection. Nano Res. 2018, 11, 2248–2255.
  26. Chen, F.; Jiang, R.; Wang, Y.; Zhu, M.; Zhang, X.; Dong, S.; Shi, H.; Wang, L. Recombinant phage elicits protective immune response against systemic s. Globosa infection in mouse model. Sci. Rep. 2017, 7, 42024.
  27. Mantile, F.; Basile, C.; Cicatiello, V.; De Falco, D.; Caivano, A.; De Berardinis, P.; Prisco, A. A multimeric immunogen for the induction of immune memory to beta-amyloid. Immunol. Cell Biol. 2011, 89, 604–609.
  28. Trovato, M.; De Berardinis, P. Novel antigen delivery systems. World J. Virol. 2015, 4, 156–168.
  29. Frenkel, D.; Katz, O.; Solomon, B. Immunization against Alzheimer’s β-amyloid plaques via EFRH phage administration. Proc. Natl. Acad. Sci. USA 2000, 97, 11455–11459.
  30. Lavie, V.; Becker, M.; Cohen-Kupiec, R.; Yacoby, I.; Koppel, R.; Wedenig, M.; Hutter-Paier, B.; Solomon, B. EFRH–Phage Immunization of Alzheimer’s Disease Animal Model Improves Behavioral Performance in Morris Water Maze Trials. J. Mol. Neurosci. 2004, 24, 105–114.
  31. Frenkel, D.; Dewachter, I.; Van Leuven, F.; Solomon, B. Reduction of beta-amyloid plaques in brain of transgenic mouse model of Alzheimer’s disease by EFRH-phage immunization. Vaccine 2003, 21, 1060–1065.
  32. Esposito, M.; Luccarini, I.; Cicatiello, V.; De Falco, D.; Fiorentini, A.; Barba, P.; Casamenti, F.; Prisco, A. Immunogenicity and therapeutic efficacy of phage-displayed beta-amyloid epitopes. Mol. Immunol. 2008, 45, 1056–1062.
  33. Castiglione, F.; Mantile, F.; De Berardinis, P.; Prisco, A. How the Interval between Prime and Boost Injection Affects the Immune Response in a Computational Model of the Immune System. Comput. Math. Methods Med. 2012, 2012, 842329.
  34. Mantile, F.; Trovato, M.; Santoni, A.; Barba, P.; Ottonello, S.; De Berardinis, P.; Prisco, A. Alum and Squalene-Oil-in-Water Emulsion Enhance the Titer and Avidity of Anti-Aβ Antibodies Induced by Multimeric Protein Antigen (1–11)E2, Preserving the Igg1-Skewed Isotype Distribution. PLoS ONE 2014, 9, e101474.
  35. Prisco, A.; De Berardinis, P. Immunogenicity of B and T epitopes displayed on bacteriophage fd. In Immunogenicity; Villanueva, C.J., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2011; pp. 205–216.
  36. Mantile, F.; Capasso, A.; De Berardinis, P.; Prisco, A. Identification of a Consolidation Phase in Immunological Memory. Front. Immunol. 2019, 10, 508.
  37. Prisco, A.; De Berardinis, P. Memory immune response: A major challenge in vaccination. Biomol. Concepts 2012, 3, 479–486.
  38. DeBerardinis, P. Recognition of HIV-derived B and T cell epitopes displayed on filamentous phages. Vaccine 1999, 17, 1434–1441.
  39. D’Apice, L.; Sartorius, R.; Caivano, A.; Mascolo, D.; Del Pozzo, G.; Di Mase, D.S.; Ricca, E.; Pira, G.L.; Manca, F.; Malanga, D.; et al. Comparative analysis of new innovative vaccine formulations based on the use of procaryotic display systems. Vaccine 2007, 25, 1993–2000.
  40. Ulivieri, C.; Citro, A.; Ivaldi, F.; Mascolo, D.; Ghittoni, R.; Fanigliulo, D.; Manca, F.; Baldari, C.T.; Li Pira, G.; Del Pozzo, G. Antigenic properties of hcmv peptides displayed by filamentous bacteriophages vs. Synthetic peptides. Immunol. Lett. 2008, 119, 62–70.
  41. Yang, Q.; Wang, L.; Lu, D.N.; Gao, R.J.; Song, J.N.; Hua, P.Y.; Yuan, D.W. Prophylactic vaccination with phage-displayed epitope of C. albicans elicits protective immune responses against systemic candidiasis in C57BL/6 mice. Vaccine 2005, 23, 4088–4096.
  42. Wang, Y.; Su, Q.; Dong, S.; Shi, H.; Gao, X.; Wang, L. Hybrid phage displaying SLAQVKYTSASSI induces protection againstCandida albicanschallenge in BALB/c mice. Hum. Vaccines Immunother. 2014, 10, 1057–1063.
  43. De Berardinis, P.; Sartorius, R.; Fanutti, C.; Perham, R.N.; Del Pozzo, G.; Guardiola, J. Phage display of peptide epitopes from HIV-1 elicits strong cytolytic responses. Nat. Biotechnol. 2000, 18, 873–876.
  44. De Berardinis, P.; Sartorius, R.; Caivano, A.; Mascolo, D.; Domingo, G.; Pozzo, G.; Gaubin, M.; Perham, R.; Piatier-Tonneau, D.; Guardiola, J. Use of Fusion Proteins and Procaryotic Display Systems for Delivery of HIV-1 Antigens: Development of Novel Vaccines for HIV-1 Infection. Curr. HIV Res. 2003, 1, 441–446.
  45. Wan, Y.; Wu, Y.; Bian, J.; Wang, X.; Zhou, W.; Jia, Z.; Tan, Y.; Zhou, L. Induction of hepatitis B virus-specific cytotoxic T lymphocytes response in vivo by filamentous phage display vaccine. Vaccine 2001, 19, 2918–2923.
  46. Mascolo, D.; Barba, P.; De Berardinis, P.; Di Rosa, F.; Del Pozzo, G. Phage display of a CTL epitope elicits a long-termin vivocytotoxic response. FEMS Immunol. Med. Microbiol. 2007, 50, 59–66.
  47. Del Pozzo, G.; Mascolo, D.; Sartorius, R.; Citro, A.; Barba, P.; D’Apice, L.; De Berardinis, P. Triggering DTH and CTL activity by fd filamentous bacteriophages: Role of CD4+ T cells in memory responses. J. Biomed. Biotechnol. 2010, 2010, 894971.
  48. Gaubin, M.; Fanutti, C.; Mishal, Z.; Durrbach, A.; De Berardinis, P.; Sartorius, R.; Del Pozzo, G.; Guardiola, J.; Perham, R.N.; Piatier-Tonneau, D. Processing of Filamentous Bacteriophage Virions in Antigen-Presenting Cells Targets Both HLA Class I and Class II Peptide Loading Compartments. DNA Cell Biol. 2003, 22, 11–18.
  49. Wan, Y.; Wu, Y.; Zhou, J.; Zou, L.; Liang, Y.; Zhao, J.; Jia, Z.; Engberg, J.; Bian, J.; Zhou, W. Cross-presentation of phage particle antigen in MHC class II and endoplasmic reticulum marker-positive compartments. Eur. J. Immunol. 2005, 35, 2041–2050.
  50. Fang, J.; Wang, G.; Yang, Q.; Song, J.; Wang, Y.; Wang, L. The potential of phage display virions expressing malignant tumor specific antigen MAGE-A1 epitope in murine model. Vaccine 2005, 23, 4860–4866.
  51. Wu, Y.; Wan, Y.; Bian, J.; Zhao, J.; Jia, Z.; Zhou, L.; Zhou, W.; Tan, Y. Phage display particles expressing tumor-specific antigens induce preventive and therapeutic anti-tumor immunity in murine p815 model. Int. J. Cancer 2002, 98, 748–753.
  52. Sartorius, R.; Pisu, P.; D’Apice, L.; Pizzella, L.; Romano, C.; Cortese, G.; Giorgini, A.; Santoni, A.; Velotti, F.; De Berardinis, P. The use of filamentous bacteriophage fd to deliver MAGE-A10 or MAGE-A3 HLA-A2-restricted peptides and to induce strong antitumor CTL responses. J. Immunol. 2008, 180, 3719–3728.
  53. Roehnisch, T.; Then, C.; Nagel, W.; Blumenthal, C.; Braciak, T.; Donzeau, M.; Böhm, T.; Flaig, M.; Bourquin, C.; Oduncu, F.S. Phage idiotype vaccination: First phase I/II clinical trial in patients with multiple myeloma. J. Transl. Med. 2014, 12, 119.
  54. Bartolacci, C.; Andreani, C.; Curcio, C.; Occhipinti, S.; Massaccesi, L.; Giovarelli, M.; Galeazzi, R.; Iezzi, M.; Tilio, M.; Gambini, V.; et al. Phage-Based Anti-HER2 Vaccination Can Circumvent Immune Tolerance against Breast Cancer. Cancer Immunol. Res. 2018, 6, 1486–1498.
  55. Eriksson, F.; Culp, W.D.; Massey, R.; Egevad, L.; Garland, D.; Persson, M.A.; Pisa, P. Tumor specific phage particles promote tumor regression in a mouse melanoma model. Cancer Immunol. Immunother. 2007, 56, 677–687.
  56. Murgas, P.; Bustamante, N.; Araya, N.; Cruz-Gomez, S.; Duran, E.; Gaete, D.; Oyarce, C.; Lopez, E.; Herrada, A.A.; Ferreira, N.; et al. A filamentous bacteriophage targeted to carcinoembryonic antigen induces tumor regression in mouse models of colorectal cancer. Cancer Immunol. Immunother. 2018, 67, 183–193.
  57. Eriksson, F.; Tsagozis, P.; Lundberg, K.; Parsa, R.; Mangsbo, S.M.; Persson, M.A.A.; Harris, R.A.; Pisa, P. Tumor-Specific Bacteriophages Induce Tumor Destruction through Activation of Tumor-Associated Macrophages. J. Immunol. 2009, 182, 3105–3111.
  58. Hashiguchi, S.; Yamaguchi, Y.; Takeuchi, O.; Akira, S.; Sugimura, K. Immunological basis of M13 phage vaccine: Regulation under MyD88 and TLR9 signaling. Biochem. Biophys. Res. Commun. 2010, 402, 19–22.
  59. Mori, K.; Kubo, T.; Kibayashi, Y.; Ohkuma, T.; Kaji, A. Anti-vaccinia virus effect of M13 bacteriophage DNA. Antivir. Res. 1996, 31, 79–86.
  60. Gomes-Neto, J.F.; Sartorius, R.; Canto, F.B.; Almeida, T.S.; Dias, A.A.; Barbosa, C.H.D.; Melo, G.A.; Oliveira, A.C.; Aguiar, P.H.N.; Machado, C.R.; et al. Vaccination With Recombinant Filamentous fd Phages Against Parasite Infection Requires TLR9 Expression. Front. Immunol. 2018, 9, 1173.
  61. Sartorius, R.; Bettua, C.; D’Apice, L.; Caivano, A.; Trovato, M.; Russo, D.; Zanoni, I.; Granucci, F.; Mascolo, D.; Barba, P.; et al. Vaccination with filamentous bacteriophages targeting DEC-205 induces DC maturation and potent anti-tumor T-cell responses in the absence of adjuvants. Eur. J. Immunol. 2011, 41, 2573–2584.
  62. Mahnke, K.; Guo, M.; Lee, S.; Sepulveda, H.; Swain, S.L.; Nussenzweig, M.; Steinman, R.M. The Dendritic Cell Receptor for Endocytosis, Dec-205, Can Recycle and Enhance Antigen Presentation via Major Histocompatibility Complex Class II–Positive Lysosomal Compartments. J. Cell Biol. 2000, 151, 673–684.
  63. Sartorius, R.; D’Apice, L.; Trovato, M.; Cuccaro, F.; Costa, V.; De Leo, M.G.; Marzullo, V.M.; Biondo, C.; D’Auria, S.; De Matteis, M.A.; et al. Antigen delivery by filamentous bacteriophage fd displaying an anti-DEC-205 single-chain variable fragment confers adjuvanticity by triggering a TLR 9-mediated immune response. EMBO Mol. Med. 2015, 7, 973–988.
  64. Krag, D.N.; Shukla, G.S.; Shen, G.P.; Pero, S.; Ashikaga, T.; Fuller, S.; Weaver, D.L.; Burdette-Radoux, S.; Thomas, C. Selection of Tumor-binding Ligands in Cancer Patients with Phage Display Libraries. Cancer Res. 2006, 66, 7724–7733.
  65. Shukla, G.S.; Krag, D.N.; Peletskaya, E.N.; Pero, S.C.; Sun, Y.J.; Carman, C.L.; McCahill, L.E.; Roland, T.A. Intravenous Infusion of Phage-displayed Antibody Library in Human Cancer Patients: Enrichment and Cancer-Specificity of Tumor-Homing Phage-Antibodies. Cancer Immunol. Immunother. 2013, 62, 1397–1410.
  66. Shadidi, M.; Sørensen, D.; Dybwad, A.; Furset, G.; Sioud, M. Mucosal vaccination with phage-displayed tumour antigens identified through proteomics-based strategy inhibits the growth and metastasis of 4T1 breast adenocarcinoma. Int. J. Oncol. 2008, 32, 241–247.
  67. Ravn, U.; Gueneau, F.; Baerlocher, L.; Osteras, M.; Desmurs, M.; Malinge, P.; Magistrelli, G.; Farinelli, L.; Kosco-Vilbois, M.H.; Fischer, N. By-passing in vitro screening—Next generation sequencing technologies applied to antibody display and in silico candidate selection. Nucleic Acids Res. 2010, 38, e193.
  68. Ghosh, D.; Kohli, A.G.; Moser, F.; Endy, D.; Belcher, A.M. Refactored M13 Bacteriophage as a Platform for Tumor Cell Imaging and Drug Delivery. ACS Synth. Biol. 2012, 1, 576–582.
  69. Lee, K.J.; Lee, J.H.; Chung, H.K.; Ju, E.J.; Song, S.Y.; Jeong, S.Y.; Choi, E.K. Application of peptide displaying phage as a novel diagnostic probe for human lung adenocarcinoma. Amino Acids 2016, 48, 1079–1086.
  70. Namdee, K.; Khongkow, M.; Boonrungsiman, S.; Nittayasut, N.; Asavarut, P.; Temisak, S.; Saengkrit, N.; Puttipipatkhachorn, S.; Hajitou, A.; Ruxrungtham, K.; et al. Thermoresponsive Bacteriophage Nanocarrier as a Gene Delivery Vector Targeted to the Gastrointestinal Tract. Mol. Ther. Nucleic Acids 2018, 12, 33–44.
  71. Bedi, D.; Gillespie, J.W.; Petrenko, V.A.; Ebner, A.; Leitner, M.; Hinterdorfer, P.; Petrenko, V.A. Targeted Delivery of siRNA into Breast Cancer Cells via Phage Fusion Proteins. Mol. Pharm. 2013, 10, 551–559.
  72. Stopar, D.; Spruijt, R.B.; Wolfs, C.J.A.M.; Hemminga, M.A. Protein–lipid interactions of bacteriophage m13 major coat protein. Biochim. Biophys. Acta (BBA) Biomembr. 2003, 1611, 5–15.
  73. Marvin, D.A.; Symmons, M.F.; Straus, S.K. Structure and assembly of filamentous bacteriophages. Prog. Biophys. Mol. Biol. 2014, 114, 80–122.
  74. Sartorius, R.; D’Apice, L.; Barba, P.; Cipria, D.; Grauso, L.; Cutignano, A.; De Berardinis, P. Vectorized Delivery of Alpha-GalactosylCeramide and Tumor Antigen on Filamentous Bacteriophage fd Induces Protective Immunity by Enhancing Tumor-Specific T Cell Response. Front. Immunol. 2018, 9, 1496.
  75. Parekh, V.V.; Wilson, M.T.; Olivares-Villagómez, D.; Singh, A.K.; Wu, L.; Wang, C.R.; Joyce, S.; Van Kaer, L. Glycolipid antigen induces long-term natural killer T cell anergy in mice. J. Clin. Investig. 2005, 115, 2572–2583.
More
Video Production Service