Designing of DNA Vaccine Based on a Secretory Form of Major Capsid Protein of Human Papillomavirus Type 18
-
Somayeh Shokri
,
Shahab Mahmoudvand
,
Manoochehr Makvandi
,
Reza Taherkhani
,
Mohammad Rashno
,
Farid Azizi Jalilian
,
Kambiz Ahmadi Angali
,
Mohammad Ali Foroughi
Abstract
More than 99% of cervical cancers are associated with human papillomaviruses (HPVs) worldwide. Current HPV vaccines are safe, highly immunogenic, with effective immunity against specific HPV types. However, DNA vaccines are a new appealing platform which can be considered for designing the HPV vaccines. This study aimed to construct a recombinant eukaryotic expression plasmid containing L1 of HPV-18, tissue plasminogen activators (tPA), and pan HLA DR-binding epitope (PADRE) genes into the pVAX1 vector.
The L1, tPA, and PADRE genes were amplified in a thermocycler. The polymerase chain reaction (PCR) products were cloned and insertion of the genes was confirmed using colony PCR, restriction enzymes analysis, and sequencing methods. Indirect immunofluorescence, RT-PCR, and western blot assays were applied to identify the target gene in HEK-293 cells. Total IgG and its isotypes in immunized mice were measured by enzyme-linked immunosorbent assay technique.
Western blot analysis showed a protein band of about 67.5 kDa in supernatant and cell lysate of transfected cells. The results of mice immunization with different constructs (group 1: the pVAX-L1, group 2: pVAX-tPA-PADRE-L1, group 3: pVAX1, and group 4: PBS as controls) indicated that the pVAX1-tPA-PADRE-L1 construct induced a significantly higher level of total IgG than pVAX1-L1 (p=0.003).
In conclusion, pVAX1-tPA-PADRE-L1 recombinant plasmid is a highly immunogenic construct and suggests as a promising candidate for vaccine development against HPV type 18 in low-middle-income countries.
1. McLaughlin-Drubin ME, Munger K. Viruses associated with human cancer. Biochim Biophys Acta. 2008;1782(3):127-50.
2. Shokri S, Mahmoudvand S, Taherkhani R, Farshadpour F, Jalalian FA. Complexity on modulation of NF‐κB pathways by hepatitis B and C: A double‐edged sword in hepatocarcinogenesis. J Cell Physiol. 2019;234(9):14734-42.
3. Garbuglia AR, Lapa D, Sias C, Capobianchi MR, Del Porto P. The Use of Both Therapeutic and Prophylactic Vaccines in the Therapy of Papillomavirus Disease. Front Immunol. 2020;11(2):188-9.
4. Mahmoudvand S, Safaei A, Erfani N, Sarvari J. Presence of human papillomavirus DNA in colorectal cancer tissues in Shiraz, Southwest Iran. Asian Pac J Cancer Prev. 2015;16(17):7883-7.
5. Rahman R, Clark M, Collins Z, Traore F, Dioukhane E, Thiam H, et al. Cervical cancer screening decentralized policy adaptation: an African rural-context-specific systematic literature review. Glob Health Action. 2019;12(1):1587894.
6. Gheit T. Mucosal and cutaneous human papillomavirus infection and cancer biology. Front Oncol. 2019;9:355.
7. Mahmoudvand S, Shokri S, Makvandi M, Taherkhani R, Rashno M, Jalilian FA, et al. In silico prediction of T‐cell and B‐cell epitopes of human papillomavirus type 16 L1 protein. Biotechnol Appl Biochem. 2021:1-12.
8. Salina Zhang B, Batur P, Ncmp C. Human papillomavirus in 2019: An update on cervical cancer prevention and screening guidelines. Cleve Clin J Med. 2019;86(3):173-8.
9. Shokri S, Shahkarami MK, Shafyi A, Mohammadi A, Esna-Ashari F, Hamta A. Evaluation of the thermal stability of live-attenuated Rubella vaccine (Takahashi strain) formulated and lyophilized in different stabilizers. J Virol Methods. 2019;264(5):18-22.
10. Zepeda-Cervantes J, Ramírez-Jarquín JO, Vaca L. Interaction Between Virus-Like Particles (VLPs) and Pattern Recognition Receptors (PRRs) From Dendritic Cells (DCs): Toward Better Engineering of VLPs. Front Immunol. 2020;11(1100).
11. Parkin DM. The global health burden of infection‐associated cancers in the year 2002. Int J Cancer. 2006;118(12):3030-44.
12. Rajčáni J, Moško T, Režuchová I. Current developments in viral DNA vaccines: shall they solve the unsolved? Rev Med Virol. 2005;15(5):303-25.
13. Fioretti D, Iurescia S, Fazio VM, Rinaldi M. DNA vaccines: developing new strategies against cancer. J Biomed Biotechnol. 2010;2010:174378.
14. Davis HL. Intramuscular and intradermal injection of DNA vaccines in mice and primates. Methods Mol Med. 2000;29:71-7.
15. Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33(4):492-503.
16. Farshadpour F, Makvandi M, Taherkhani R. Design, construction and cloning of truncated ORF2 and tPAsp-PADRE-truncated ORF2 gene cassette from hepatitis E virus in the pVAX1 expression vector. Jundishapur J Microbiol. 2015;8(12):e26035.
17. Farshadpour F, Taherkhani R, Makvandi M, Rajabi Memari H, Samarbafzadeh AR. Codon-Optimized Expression and Purification of Truncated ORF2 Protein of Hepatitis E Virus in Escherichia coli. Jundishapur J Microbiol. 2014;7(7):e11261-e.
18. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-54.
19. Lladser A, Párraga M, Quevedo L, Molina MC, Silva S, Ferreira A, et al. Naked DNA immunization as an approach to target the generic tumor antigen survivin induces humoral and cellular immune responses in mice. Immunobiology. 2006;211(1-2):11-27.
20. Taherkhani R, Makvandi M, Farshadpour F. Development of enzyme-linked immunosorbent assays using 2 truncated ORF2 proteins for detection of IgG antibodies against hepatitis E virus. Ann Lab Med. 2014;34(2):118-26.
21. Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer Observatory: cancer today. Lyon, France: international agency for research on cancer. Cancer Today. 2018.
22. Yin F, Wang Y, Chen N, Jiang D, Qiu Y, Wang Y, et al. A novel trivalent HPV 16/18/58 vaccine with anti-HPV 16 and 18 neutralizing antibody responses comparable to those induced by the Gardasil quadrivalent vaccine in rhesus macaque model. Papillomavirus Res. 2017;3(1):85-90.
23. Madrid-Marina V, Torres-Poveda K, López-Toledo G, García-Carrancá A. Advantages and Disadvantages of Current Prophylactic Vaccines Against HPV. Arch Med Res. 2009;40(6):471-7.
24. Cheng MA, Farmer E, Huang C, Lin J, Hung C-F, Wu TC. Therapeutic DNA Vaccines for Human Papillomavirus and Associated Diseases. Hum Gene Ther. 2018;29(9):971-96.
25. Sanina N. Vaccine Adjuvants Derived from Marine Organisms. Biomolecules. 2019;9(8):340.
26. Kim D, Hoory T, Monie A, Ting JP-Y, Hung C-F, Wu TC. Enhancement of DNA vaccine potency through coadministration of CIITA DNA with DNA vaccines via gene gun. J Immunol. 2008;180(10):7019-27.
27. Taherkhani R, Farshadpour F, Makvandi M, Rajabi Memari H, Samarbafzadeh AR, Sharifi N, et al. Cytokine Profiles and Cell Proliferation Responses to Truncated ORF2 Protein in Iranian Patients Recovered from Hepatitis E Infection. J Trop Med. 2015;2015:523560.
28. Taherkhani R, Farshadpour F, Makvandi M. Design and production of a multiepitope construct derived from hepatitis E virus capsid protein. J Med Virol. 2015;87(7):1225-34.
29. Rosa DS, Tzelepis F, Cunha MG, Soares IS, Rodrigues MM. The pan HLA DR-binding epitope improves adjuvant-assisted immunization with a recombinant protein containing a malaria vaccine candidate. Immunol Lett. 2004;92(3):259-68.
30. Gholizadeh Z, Tavakkol‐Afshari J, Nikpoor AR, Jalali SA, Jaafari MR. Enhanced immune response induced by P5 HER2/neu‐derived peptide‐pulsed dendritic cells as a preventive cancer vaccine. J Cell Mol Med. 2018;22(1):558-67.
31. Makvandi M, Taherkhani R, Azizolahi B. Cloning and Expression of a Secretory form of Truncated ORF2 (aa 112-607) from Hepatitis E Virus in the pVAX1 Vector. Jundishapur J Microbiol. 2017;10(11):e13543.
32. Wang G, Pan L, Zhang Y. Approaches to improved targeting of DNA vaccines. Hum Vaccin. 2011;7(12):1271-81.
33. Tsen S-WD, Paik AH, Hung C-F, Wu TC. Enhancing DNA vaccine potency by modifying the properties of antigen-presenting cells. Expert Rev Vaccines. 2007;6(2):227-39.
34. Weinberger EE, Isakovic A, Scheiblhofer S, Ramsauer C, Reiter K, Hauser-Kronberger C, et al. The influence of antigen targeting to sub-cellular compartments on the anti-allergic potential of a DNA vaccine. Vaccine. 2013;31(51):6113-21.
35. Midha S, Bhatnagar R. Anthrax protective antigen administered by DNA vaccination to distinct subcellular locations potentiates humoral and cellular immune responses. Eur J Immunol. 2009;39(1):159-77.
36. Ashok MS, Rangarajan PN. Protective efficacy of a plasmid DNA encoding Japanese encephalitis virus envelope protein fused to tissue plasminogen activator signal sequences: studies in a murine intracerebral virus challenge model. Vaccine. 2002;20(11-12):1563-70.
37. Liang R, Van den Hurk JV, Zheng C, Yu H, Pontarollo RA, Babiuk LA. Immunization with plasmid DNA encoding a truncated, secreted form of the bovine viral diarrhea virus E2 protein elicits strong humoral and cellular immune responses. Vaccine. 2005;23(45):5252-62.
38. Luo M, Tao P, Li J, Zhou S, Guo D, Pan Z. Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods. 2008;154(1):121-7.
39. Kim SJ, Suh D, Park SE, Park J-S, Byun H-M, Lee C, et al. Enhanced immunogenicity of DNA fusion vaccine encoding secreted hepatitis B surface antigen and chemokine RANTES. Virology. 2003;314(1):84-91.
40. Li J, Liang Q, Song W, Marchisio MA. Nucleotides upstream of the Kozak sequence strongly influence gene expression in the yeast S. cerevisiae. J Biol Eng. 2017;11(1):25-9.
41. Hasanzadeh S, Habibi M, Shokrgozar MA, Ahangari Cohan R, Ahmadi K, Asadi Karam MR, et al. In silico analysis and in vivo assessment of a novel epitope-based vaccine candidate against uropathogenic Escherichia coli. Sci Rep. 2020;10(1):16258-62.
42. Daifalla NS, Bayih AG, Gedamu L. Differential Immune Response against Recombinant Leishmania donovani Peroxidoxin 1 and Peroxidoxin 2 Proteins in BALB/c Mice. J Immunol Res. 2015;2015:348401.
43. Kim D, Hoory T, Wu T-C, Hung C-F. Enhancing DNA vaccine potency by combining a strategy to prolong dendritic cell life and intracellular targeting strategies with a strategy to boost CD4+ T cells. Hum Gene Ther. 2007;18(11):1129-40.
44. Yang B, Yang A, Peng S, Pang X, Roden RBS, Wu TC, et al. Co-administration with DNA encoding papillomavirus capsid proteins enhances the antitumor effects generated by therapeutic HPV DNA vaccination. Cell Biosci. 2015;5(1):35-8.
45. Rose RC, Lane C, Wilson S, Suzich JA, Rybicki E, Williamson A-L. Oral vaccination of mice with human papillomavirus virus-like particles induces systemic virus-neutralizing antibodies. Vaccine. 1999;17(17):2129-35.
46. Gerber S, Lane C, Brown DM, Lord E, DiLorenzo M, Clements J, et al. Human papillomavirus virus-like particles are efficient oral immunogens when coadministered with Escherichia coli heat-labile enterotoxin mutant R192G or CpG DNA. J Virol. 2001;75(10):4752-60.
47. Kim S, Lee C, Lee S, Kim I, Park J, Sasagawa T, et al. Enhanced immunogenicity of human papillomavirus 16 L1 genetic vaccines fused to an ER-targeting secretory signal peptide and RANTES. Gene Ther. 2003;10(15):1268-73.
48. Hung C-F, Tsai Y-C, He L, Wu TC. DNA Vaccines Encoding Ii-PADRE Generates Potent PADRE-specific CD4+ T-Cell Immune Responses and Enhances Vaccine Potency. Mol Ther. 2007;15(6):1211-9.
49. Ghaffari-Nazari H, Tavakkol-Afshari J, Jaafari MR, Tahaghoghi-Hajghorbani S, Masoumi E, Jalali SA. Improving Multi-Epitope Long Peptide Vaccine Potency by Using a Strategy that Enhances CD4+ T Help in BALB/c Mice. PLoS One. 2015;10(11):e0142563.
50. Hung C-F, Tsai Y-C, He L, Wu TC. DNA vaccines encoding Ii-PADRE generates potent PADRE-specific CD4+ T-cell immune responses and enhances vaccine potency. Mol Ther. 2007;15(6):1211-9.
51. Wu A, Zeng Q, Kang TH, Peng S, Roosinovich E, Pai SI, et al. Innovative DNA vaccine for human papillomavirus (HPV)-associated head and neck cancer. Gene Ther. 2011;18(3):304-12.
52. Kim D, Hoory T, Monie A, Ting JP, Hung CF, Wu TC. Enhancement of DNA vaccine potency through coadministration of CIITA DNA with DNA vaccines via gene gun. J Immunol. 2008;180(10):7019-27.
53. Dan X, Han L, Riaz H, Luo X, Liu X, Chong Z, et al. Construction and evaluation of the novel DNA vaccine harboring the inhibin α (1-32) and the RF-amide related peptide-3 genes for improving fertility in mice. Exp Anim. 2016;65(1):17-25.
54. Delogu G, Li A, Repique C, Collins F, Morris SL. DNA vaccine combinations expressing either tissue plasminogen activator signal sequence fusion proteins or ubiquitin-conjugated antigens induce sustained protective immunity in a mouse model of pulmonary tuberculosis. Infect Immun. 2002;70(1):292-302.
55. Luo M, Tao P, Li J, Zhou S, Guo D, Pan Z. Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods. 2008;154(1-2):121-7.
56. Hanke T, Ondondo B, Abdul-Jawad S, Roshorm Y, Bridgeman A. Vector delivery-dependant effect of human tissue plasminogen activator signal peptide on vaccine induction of T cells. Journal of HIV and AIDS. 2016.
57. Haddad D, Liljeqvist S, Ståhl S, Andersson I, Perlmann P, Berzins K, et al. Comparative study of DNA-based immunization vectors: effect of secretion signals on the antibody responses in mice. FEMS Immunol Med Microbiol 1997;18(3):193-202.
2. Shokri S, Mahmoudvand S, Taherkhani R, Farshadpour F, Jalalian FA. Complexity on modulation of NF‐κB pathways by hepatitis B and C: A double‐edged sword in hepatocarcinogenesis. J Cell Physiol. 2019;234(9):14734-42.
3. Garbuglia AR, Lapa D, Sias C, Capobianchi MR, Del Porto P. The Use of Both Therapeutic and Prophylactic Vaccines in the Therapy of Papillomavirus Disease. Front Immunol. 2020;11(2):188-9.
4. Mahmoudvand S, Safaei A, Erfani N, Sarvari J. Presence of human papillomavirus DNA in colorectal cancer tissues in Shiraz, Southwest Iran. Asian Pac J Cancer Prev. 2015;16(17):7883-7.
5. Rahman R, Clark M, Collins Z, Traore F, Dioukhane E, Thiam H, et al. Cervical cancer screening decentralized policy adaptation: an African rural-context-specific systematic literature review. Glob Health Action. 2019;12(1):1587894.
6. Gheit T. Mucosal and cutaneous human papillomavirus infection and cancer biology. Front Oncol. 2019;9:355.
7. Mahmoudvand S, Shokri S, Makvandi M, Taherkhani R, Rashno M, Jalilian FA, et al. In silico prediction of T‐cell and B‐cell epitopes of human papillomavirus type 16 L1 protein. Biotechnol Appl Biochem. 2021:1-12.
8. Salina Zhang B, Batur P, Ncmp C. Human papillomavirus in 2019: An update on cervical cancer prevention and screening guidelines. Cleve Clin J Med. 2019;86(3):173-8.
9. Shokri S, Shahkarami MK, Shafyi A, Mohammadi A, Esna-Ashari F, Hamta A. Evaluation of the thermal stability of live-attenuated Rubella vaccine (Takahashi strain) formulated and lyophilized in different stabilizers. J Virol Methods. 2019;264(5):18-22.
10. Zepeda-Cervantes J, Ramírez-Jarquín JO, Vaca L. Interaction Between Virus-Like Particles (VLPs) and Pattern Recognition Receptors (PRRs) From Dendritic Cells (DCs): Toward Better Engineering of VLPs. Front Immunol. 2020;11(1100).
11. Parkin DM. The global health burden of infection‐associated cancers in the year 2002. Int J Cancer. 2006;118(12):3030-44.
12. Rajčáni J, Moško T, Režuchová I. Current developments in viral DNA vaccines: shall they solve the unsolved? Rev Med Virol. 2005;15(5):303-25.
13. Fioretti D, Iurescia S, Fazio VM, Rinaldi M. DNA vaccines: developing new strategies against cancer. J Biomed Biotechnol. 2010;2010:174378.
14. Davis HL. Intramuscular and intradermal injection of DNA vaccines in mice and primates. Methods Mol Med. 2000;29:71-7.
15. Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33(4):492-503.
16. Farshadpour F, Makvandi M, Taherkhani R. Design, construction and cloning of truncated ORF2 and tPAsp-PADRE-truncated ORF2 gene cassette from hepatitis E virus in the pVAX1 expression vector. Jundishapur J Microbiol. 2015;8(12):e26035.
17. Farshadpour F, Taherkhani R, Makvandi M, Rajabi Memari H, Samarbafzadeh AR. Codon-Optimized Expression and Purification of Truncated ORF2 Protein of Hepatitis E Virus in Escherichia coli. Jundishapur J Microbiol. 2014;7(7):e11261-e.
18. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-54.
19. Lladser A, Párraga M, Quevedo L, Molina MC, Silva S, Ferreira A, et al. Naked DNA immunization as an approach to target the generic tumor antigen survivin induces humoral and cellular immune responses in mice. Immunobiology. 2006;211(1-2):11-27.
20. Taherkhani R, Makvandi M, Farshadpour F. Development of enzyme-linked immunosorbent assays using 2 truncated ORF2 proteins for detection of IgG antibodies against hepatitis E virus. Ann Lab Med. 2014;34(2):118-26.
21. Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer Observatory: cancer today. Lyon, France: international agency for research on cancer. Cancer Today. 2018.
22. Yin F, Wang Y, Chen N, Jiang D, Qiu Y, Wang Y, et al. A novel trivalent HPV 16/18/58 vaccine with anti-HPV 16 and 18 neutralizing antibody responses comparable to those induced by the Gardasil quadrivalent vaccine in rhesus macaque model. Papillomavirus Res. 2017;3(1):85-90.
23. Madrid-Marina V, Torres-Poveda K, López-Toledo G, García-Carrancá A. Advantages and Disadvantages of Current Prophylactic Vaccines Against HPV. Arch Med Res. 2009;40(6):471-7.
24. Cheng MA, Farmer E, Huang C, Lin J, Hung C-F, Wu TC. Therapeutic DNA Vaccines for Human Papillomavirus and Associated Diseases. Hum Gene Ther. 2018;29(9):971-96.
25. Sanina N. Vaccine Adjuvants Derived from Marine Organisms. Biomolecules. 2019;9(8):340.
26. Kim D, Hoory T, Monie A, Ting JP-Y, Hung C-F, Wu TC. Enhancement of DNA vaccine potency through coadministration of CIITA DNA with DNA vaccines via gene gun. J Immunol. 2008;180(10):7019-27.
27. Taherkhani R, Farshadpour F, Makvandi M, Rajabi Memari H, Samarbafzadeh AR, Sharifi N, et al. Cytokine Profiles and Cell Proliferation Responses to Truncated ORF2 Protein in Iranian Patients Recovered from Hepatitis E Infection. J Trop Med. 2015;2015:523560.
28. Taherkhani R, Farshadpour F, Makvandi M. Design and production of a multiepitope construct derived from hepatitis E virus capsid protein. J Med Virol. 2015;87(7):1225-34.
29. Rosa DS, Tzelepis F, Cunha MG, Soares IS, Rodrigues MM. The pan HLA DR-binding epitope improves adjuvant-assisted immunization with a recombinant protein containing a malaria vaccine candidate. Immunol Lett. 2004;92(3):259-68.
30. Gholizadeh Z, Tavakkol‐Afshari J, Nikpoor AR, Jalali SA, Jaafari MR. Enhanced immune response induced by P5 HER2/neu‐derived peptide‐pulsed dendritic cells as a preventive cancer vaccine. J Cell Mol Med. 2018;22(1):558-67.
31. Makvandi M, Taherkhani R, Azizolahi B. Cloning and Expression of a Secretory form of Truncated ORF2 (aa 112-607) from Hepatitis E Virus in the pVAX1 Vector. Jundishapur J Microbiol. 2017;10(11):e13543.
32. Wang G, Pan L, Zhang Y. Approaches to improved targeting of DNA vaccines. Hum Vaccin. 2011;7(12):1271-81.
33. Tsen S-WD, Paik AH, Hung C-F, Wu TC. Enhancing DNA vaccine potency by modifying the properties of antigen-presenting cells. Expert Rev Vaccines. 2007;6(2):227-39.
34. Weinberger EE, Isakovic A, Scheiblhofer S, Ramsauer C, Reiter K, Hauser-Kronberger C, et al. The influence of antigen targeting to sub-cellular compartments on the anti-allergic potential of a DNA vaccine. Vaccine. 2013;31(51):6113-21.
35. Midha S, Bhatnagar R. Anthrax protective antigen administered by DNA vaccination to distinct subcellular locations potentiates humoral and cellular immune responses. Eur J Immunol. 2009;39(1):159-77.
36. Ashok MS, Rangarajan PN. Protective efficacy of a plasmid DNA encoding Japanese encephalitis virus envelope protein fused to tissue plasminogen activator signal sequences: studies in a murine intracerebral virus challenge model. Vaccine. 2002;20(11-12):1563-70.
37. Liang R, Van den Hurk JV, Zheng C, Yu H, Pontarollo RA, Babiuk LA. Immunization with plasmid DNA encoding a truncated, secreted form of the bovine viral diarrhea virus E2 protein elicits strong humoral and cellular immune responses. Vaccine. 2005;23(45):5252-62.
38. Luo M, Tao P, Li J, Zhou S, Guo D, Pan Z. Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods. 2008;154(1):121-7.
39. Kim SJ, Suh D, Park SE, Park J-S, Byun H-M, Lee C, et al. Enhanced immunogenicity of DNA fusion vaccine encoding secreted hepatitis B surface antigen and chemokine RANTES. Virology. 2003;314(1):84-91.
40. Li J, Liang Q, Song W, Marchisio MA. Nucleotides upstream of the Kozak sequence strongly influence gene expression in the yeast S. cerevisiae. J Biol Eng. 2017;11(1):25-9.
41. Hasanzadeh S, Habibi M, Shokrgozar MA, Ahangari Cohan R, Ahmadi K, Asadi Karam MR, et al. In silico analysis and in vivo assessment of a novel epitope-based vaccine candidate against uropathogenic Escherichia coli. Sci Rep. 2020;10(1):16258-62.
42. Daifalla NS, Bayih AG, Gedamu L. Differential Immune Response against Recombinant Leishmania donovani Peroxidoxin 1 and Peroxidoxin 2 Proteins in BALB/c Mice. J Immunol Res. 2015;2015:348401.
43. Kim D, Hoory T, Wu T-C, Hung C-F. Enhancing DNA vaccine potency by combining a strategy to prolong dendritic cell life and intracellular targeting strategies with a strategy to boost CD4+ T cells. Hum Gene Ther. 2007;18(11):1129-40.
44. Yang B, Yang A, Peng S, Pang X, Roden RBS, Wu TC, et al. Co-administration with DNA encoding papillomavirus capsid proteins enhances the antitumor effects generated by therapeutic HPV DNA vaccination. Cell Biosci. 2015;5(1):35-8.
45. Rose RC, Lane C, Wilson S, Suzich JA, Rybicki E, Williamson A-L. Oral vaccination of mice with human papillomavirus virus-like particles induces systemic virus-neutralizing antibodies. Vaccine. 1999;17(17):2129-35.
46. Gerber S, Lane C, Brown DM, Lord E, DiLorenzo M, Clements J, et al. Human papillomavirus virus-like particles are efficient oral immunogens when coadministered with Escherichia coli heat-labile enterotoxin mutant R192G or CpG DNA. J Virol. 2001;75(10):4752-60.
47. Kim S, Lee C, Lee S, Kim I, Park J, Sasagawa T, et al. Enhanced immunogenicity of human papillomavirus 16 L1 genetic vaccines fused to an ER-targeting secretory signal peptide and RANTES. Gene Ther. 2003;10(15):1268-73.
48. Hung C-F, Tsai Y-C, He L, Wu TC. DNA Vaccines Encoding Ii-PADRE Generates Potent PADRE-specific CD4+ T-Cell Immune Responses and Enhances Vaccine Potency. Mol Ther. 2007;15(6):1211-9.
49. Ghaffari-Nazari H, Tavakkol-Afshari J, Jaafari MR, Tahaghoghi-Hajghorbani S, Masoumi E, Jalali SA. Improving Multi-Epitope Long Peptide Vaccine Potency by Using a Strategy that Enhances CD4+ T Help in BALB/c Mice. PLoS One. 2015;10(11):e0142563.
50. Hung C-F, Tsai Y-C, He L, Wu TC. DNA vaccines encoding Ii-PADRE generates potent PADRE-specific CD4+ T-cell immune responses and enhances vaccine potency. Mol Ther. 2007;15(6):1211-9.
51. Wu A, Zeng Q, Kang TH, Peng S, Roosinovich E, Pai SI, et al. Innovative DNA vaccine for human papillomavirus (HPV)-associated head and neck cancer. Gene Ther. 2011;18(3):304-12.
52. Kim D, Hoory T, Monie A, Ting JP, Hung CF, Wu TC. Enhancement of DNA vaccine potency through coadministration of CIITA DNA with DNA vaccines via gene gun. J Immunol. 2008;180(10):7019-27.
53. Dan X, Han L, Riaz H, Luo X, Liu X, Chong Z, et al. Construction and evaluation of the novel DNA vaccine harboring the inhibin α (1-32) and the RF-amide related peptide-3 genes for improving fertility in mice. Exp Anim. 2016;65(1):17-25.
54. Delogu G, Li A, Repique C, Collins F, Morris SL. DNA vaccine combinations expressing either tissue plasminogen activator signal sequence fusion proteins or ubiquitin-conjugated antigens induce sustained protective immunity in a mouse model of pulmonary tuberculosis. Infect Immun. 2002;70(1):292-302.
55. Luo M, Tao P, Li J, Zhou S, Guo D, Pan Z. Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods. 2008;154(1-2):121-7.
56. Hanke T, Ondondo B, Abdul-Jawad S, Roshorm Y, Bridgeman A. Vector delivery-dependant effect of human tissue plasminogen activator signal peptide on vaccine induction of T cells. Journal of HIV and AIDS. 2016.
57. Haddad D, Liljeqvist S, Ståhl S, Andersson I, Perlmann P, Berzins K, et al. Comparative study of DNA-based immunization vectors: effect of secretion signals on the antibody responses in mice. FEMS Immunol Med Microbiol 1997;18(3):193-202.
| Files | ||
| Issue | Vol 20 No 5 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v20i5.7403 | |
| Keywords | ||
| Alphapapillomaviruses DNA vaccines Indirect fluorescent antibody technique Polymerase chain reaction Uterine cervical neoplasms Western blotting | ||
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How to Cite
1.
Shokri S, Mahmoudvand S, Makvandi M, Taherkhani R, Rashno M, Azizi Jalilian F, Ahmadi Angali K, Foroughi MA. Designing of DNA Vaccine Based on a Secretory Form of Major Capsid Protein of Human Papillomavirus Type 18. Iran J Allergy Asthma Immunol. 2021;20(5):525-536.
