565
Views
32
CrossRef citations to date
0
Altmetric
Research Articles

Exploring the cancer-testis antigen BORIS to design a novel multi-epitope vaccine against breast cancer based on immunoinformatics approaches

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , & show all
Pages 6363-6380 | Received 13 Jul 2020, Accepted 25 Jan 2021, Published online: 18 Feb 2021

References

  • Abbosh, C., Birkbak, N. J., Wilson, G. A., Jamal-Hanjani, M., Constantin, T., Salari, R., Le Quesne, J., Moore, D. A., Veeriah, S., Rosenthal, R., Marafioti, T., Kirkizlar, E., Watkins, T. B. K., McGranahan, N., Ward, S., Martinson, L., Riley, J., Fraioli, F., Al Bakir, M., … Swanton, C. (2017). Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature, 545(7655), 446–451. https://doi.org/10.1038/nature22364
  • Abdelmoneim, A. H. (2020). Immunoinformatics design of multiepitopes peptide-based universal cancer vaccine using matrix metalloproteinase-9 protein as a target. Immunological Medicine, 1–18. https://doi.org/10.1080/25785826.2020.1794165
  • Adhikari, U. K., Tayebi, M., & Rahman, M. M. (2018). Immunoinformatics approach for epitope-based peptide vaccine design and active site prediction against polyprotein of emerging Oropouche virus. Journal of Immunology Research, 2018, 6718083. https://doi.org/10.1155/2018/6718083
  • Agallou, M., Athanasiou, E., Koutsoni, O., Dotsika, E., & Karagouni, E. (2014). Experimental validation of multi-epitope peptides including promising MHC class I- and II-Restricted Epitopes of four known Leishmania infantum proteins. Frontiers in Immunology, 5, 268. https://doi.org/10.3389/fimmu.2014.00268
  • Agallou, M., Margaroni, M., Kotsakis, S. D., & Karagouni, E. (2020). A canine-directed chimeric multi-epitope vaccine induced protective immune responses in BALB/c mice infected with Leishmania infantum. Vaccines, 8(3), 350. https://doi.org/10.3390/vaccines8030350
  • Ahmad, I. (2020). Development of multi-epitope subunit vaccine for protection against the norovirus’ infections based on computational vaccinology. Journal of Biomolecular Structure and Dynamics, 1.–12. https://doi.org/10.1080/07391102.2020.1845799
  • Alberti, L. (2015). Different effects of BORIS/CTCFL on stemness gene expression, sphere formation and cell survival in epithelial cancer stem cells. PLoS One, 10(7), e0132977. https://doi.org/10.1371/journal.pone.0132977
  • Ang, X. L., & Harper, J. W. (2005). SCF-mediated protein degradation and cell cycle control. Oncogene, 24(17), 2860–2870. https://doi.org/10.1038/sj.onc.1208614
  • Arai, R., Ueda, H., Kitayama, A., Kamiya, N., & Nagamune, T. (2001). Design of the linkers which effectively separate domains of a bifunctional fusion protein. Protein Engineering, 14(8), 529–532. https://doi.org/10.1093/protein/14.8.529
  • Asano, T., Hirohashi, Y., Torigoe, T., Mariya, T., Horibe, R., Kuroda, T., Tabuchi, Y., Saijo, H., Yasuda, K., Mizuuchi, M., Takahashi, A., Asanuma, H., Hasegawa, T., Saito, T., & Sato, N. (2016). Brother of the regulator of the imprinted site (BORIS) variant subfamily 6 is involved in cervical cancer stemness and can be a target of immunotherapy. Oncotarget, 7(10), 11223–11237. https://doi.org/10.18632/oncotarget.7165
  • Bhasin, M., & Raghava, G. (2004a). Analysis and prediction of affinity of TAP binding peptides using cascade SVM. Protein Science: A Publication of the Protein Society, 13(3), 596–607. https://doi.org/10.1110/ps.03373104
  • Bhasin, M., & Raghava, G. (2004b). Prediction of CTL epitopes using QM, SVM and ANN techniques. Vaccine, 22(23-24), 3195–3204. https://doi.org/10.1016/j.vaccine.2004.02.005
  • Blattman, J. N., & Greenberg, P. D. (2004). Cancer immunotherapy: A treatment for the masses. Science (New York, N.Y.), 305(5681), 200–205. https://doi.org/10.1126/science.1100369
  • Blom, N., Gammeltoft, S., & Brunak, S. (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology, 294(5), 1351–1362. https://doi.org/10.1006/jmbi.1999.3310
  • Blum, J. S., Wearsch, P. A., & Cresswell, P. (2013). Pathways of antigen processing. Annual Review of Immunology, 31, 443–473. https://doi.org/10.1146/annurev-immunol-032712-095910
  • Briesemeister, S., Blum, T., Brady, S., Lam, Y., Kohlbacher, O., & Shatkay, H. (2009). SherLoc2: A high-accuracy hybrid method for predicting subcellular localization of proteins. Journal of Proteome Research, 8(11), 5363–5366. https://doi.org/10.1021/pr900665y
  • Brusic, V., & Petrovsky, N. (2005). Immunoinformatics and its relevance to understanding human immune disease. Expert Review of Clinical Immunology, 1(1), 145–157. https://doi.org/10.1586/1744666X.1.1.145
  • Cai, C. Z., Han, L. Y., Ji, Z. L., Chen, X., & Chen, Y. Z. (2003). SVM-Prot: Web-based support vector machine software for functional classification of a protein from its primary sequence. Nucleic Acids Research, 31(13), 3692–3697. https://doi.org/10.1093/nar/gkg600
  • Cappello, P., & Novelli, F. (2017). Next generation of cancer immunotherapy calls for combination. Oncoscience, 4(3-4), 19–20. https://doi.org/10.18632/oncoscience.343
  • Castro, F., Cardoso, A. P., Gonçalves, R. M., Serre, K., & Oliveira, M. J. (2018). Interferon-gamma at the crossroads of tumor immune surveillance or evasion. Frontiers in Immunology, 9, 847. https://doi.org/10.3389/fimmu.2018.00847
  • Cerezo, D., Peña, M. J., Mijares, M., Martínez, G., Blanca, I., & De Sanctis, J. B. (2015). Peptide vaccines for cancer therapy. Recent Patents on Inflammation & Allergy Drug Discovery, 9(1), 38–45. https://doi.org/10.2174/1872213x09666150131141953
  • Chakraborty, I., Bodurtha, K. J., Heeder, N. J., Godfrin, M. P., Tripathi, A., Hurt, R. H., Shukla, A., & Bose, A. (2014). Massive electrical conductivity enhancement of multilayer graphene/polystyrene composites using a nonconductive filler. ACS Applied Materials & Interfaces, 6(19), 16472–16475. https://doi.org/10.1021/am5044592
  • Chakraborty, S., & Rahman, T. (2012). The difficulties in cancer treatment. Ecancermedicalscience, 6.
  • Cheema, Z., Hari-Gupta, Y., Kita, G.-X., Farrar, D., Seddon, I., Corr, J., & Klenova, E. (2014). Expression of the cancer-testis antigen BORIS correlates with prostate cancer. The Prostate, 74(2), 164–176. https://doi.org/10.1002/pros.22738
  • Chen, P., Rayner, S., & Hu, K. (2011). Advances of bioinformatics tools applied in virus epitopes prediction. Virologica Sinica, 26(1), 1–7. https://doi.org/10.1007/s12250-011-3159-4
  • Chen, X., Zaro, J. L., & Shen, W.-C. (2013). Fusion protein linkers: Property, design and functionality. Advanced Drug Delivery Reviews, 65(10), 1357–1369. https://doi.org/10.1016/j.addr.2012.09.039
  • Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science: A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
  • Comeau, S. R., Gatchell, D. W., Vajda, S., & Camacho, C. J. (2004a). ClusPro: An automated docking and discrimination method for the prediction of protein complexes. Bioinformatics (Oxford, England), 20(1), 45–50. https://doi.org/10.1093/bioinformatics/btg371
  • Comeau, S. R., Gatchell, D. W., Vajda, S., & Camacho, C. J. (2004b). ClusPro: A fully automated algorithm for protein-protein docking. Nucleic Acids Research, 32(Web Server issue), W96–W99. https://doi.org/10.1093/nar/gkh354
  • Costello, R. T., Gastaut, J. A., & Olive, D. (1999). Tumor escape from immune surveillance. Archivum Immunologiae et Therapiae Experimentalis, 47(2), 83–88.
  • Dhanda, S. K., Karosiene, E., Edwards, L., Grifoni, A., Paul, S., Andreatta, M., Weiskopf, D., Sidney, J., Nielsen, M., Peters, B., & Sette, A. (2018). Predicting HLA CD4 immunogenicity in human populations. Frontiers in Immunology, 9, 1369. https://doi.org/10.3389/fimmu.2018.01369
  • Dougan, D., Micevski, D., & Truscott, K. (2012). The N-end rule pathway: From recognition by N-recognins, to destruction by AAA + proteases. Biochimica et Biophysica Acta, 1823(1), 83–91. https://doi.org/10.1016/j.bbamcr.2011.07.002
  • Doytchinova, I. A., & Flower, D. R. (2008). Bioinformatic approach for identifying parasite and fungal candidate subunit vaccines. The Open Vaccine Journal, 1(1), 22-26.
  • Duan, G., & Walther, D. (2015). The roles of post-translational modifications in the context of protein interaction networks. PLOS Computational Biology, 11(2), e1004049. https://doi.org/10.1371/journal.pcbi.1004049
  • EL-Manzalawy, Y., Dobbs, D., & Honavar, V. (2008). Predicting linear B-cell epitopes using string kernels. Journal of Molecular Recognition, 21(4), 243–255. https://doi.org/10.1002/jmr.893
  • Ebert, L. M., Liu, Y. C., Clements, C. S., Robson, N. C., Jackson, H. M., Markby, J. L., Dimopoulos, N., Tan, B. S., Luescher, I. F., Davis, I. D., Rossjohn, J., Cebon, J., Purcell, A. W., & Chen, W. (2009). A long, naturally presented immunodominant epitope from NY-ESO-1 tumor antigen: Implications for cancer vaccine design. Cancer Research, 69(3), 1046–1054. https://doi.org/10.1158/0008-5472.CAN-08-2926
  • Ehx, G., & Perreault, C. (2019). Discovery and characterization of actionable tumor antigens. Genome Medicine, 11(1), 29. https://doi.org/10.1186/s13073-019-0642-x
  • Farhadi, T., & Ranjbar, M. (2017). Designing and modeling of complex DNA vaccine based on MOMP of Chlamydia trachomatis: An in silico approach. Network Modeling Analysis in Health Informatics and Bioinformatics, 6(1), 1.
  • Farhood, B., Najafi, M., & Mortezaee, K. (2019). CD8+ cytotoxic T lymphocytes in cancer immunotherapy: A review. The Journal of Cellular Physiology, 234(6), 8509–8521. https://doi.org/10.1002/jcp.27782
  • Ferro, S., Huber, V., & Rivoltini, L. (2018). Mechanisms of tumor immunotherapy, with a focus on thoracic cancers. Journal of Thoracic Disease, 10(7), 4619–4631. https://doi.org/10.21037/jtd.2018.07.30
  • Fonseca, J. A., Cabrera-Mora, M., Kashentseva, E. A., Villegas, J. P., Fernandez, A., Van Pelt, A., Dmitriev, I. P., Curiel, D. T., & Moreno, A. (2016). A plasmodium promiscuous T cell epitope delivered within the Ad5 hexon protein enhances the protective efficacy of a protein based malaria vaccine. PLoS One, 11(4), e0154819. https://doi.org/10.1371/journal.pone.0154819
  • Fratta, E., Coral, S., Covre, A., Parisi, G., Colizzi, F., Danielli, R., Nicolay, H. J. M., Sigalotti, L., & Maio, M. (2011). The biology of cancer testis antigens: Putative function, regulation and therapeutic potential. Molecular Oncology, 5(2), 164–182. https://doi.org/10.1016/j.molonc.2011.02.001
  • Gao, D., Chen, Y., Han, D., Qi, Q., Sun, X., Zhang, H., Feng, H., & Wang, M. (2017). Membrane-anchored stalk domain of influenza HA enhanced immune responses in mice. Microbial Pathogenesis, 113, 421–426. https://doi.org/10.1016/j.micpath.2017.11.025
  • Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In The proteomics protocols handbook (pp. 571–607). Springer.
  • Ghaffari-Nazari, H., Tavakkol-Afshari, J., Jaafari, M. R., Tahaghoghi-Hajghorbani, S., Masoumi, E., & Jalali, S. A. (2015). Improving multi-epitope long peptide vaccine potency by using a strategy that enhances CD4+ T help in BALB/c mice. PLoS One, 10(11), e0142563. https://doi.org/10.1371/journal.pone.0142563
  • Ghafourifard, S., & Modaresi, M. (2009). Cancer-testis antigens: Potential targets for cancer immunotherapy. Archives of Iranian Medicine, 12(4), 395–404.
  • Ghahremani, F., Kefayat, A., Shahbazi-Gahrouei, D., Motaghi, H., Mehrgardi, M. A., & Haghjooy-Javanmard, S. (2018). AS1411 aptamer-targeted gold nanoclusters effect on the enhancement of radiation therapy efficacy in breast tumor-bearing mice. Nanomedicine (London, England), 13(20), 2563–2578. https://doi.org/10.2217/nnm-2018-0180
  • Ghahremani, F., Shahbazi-Gahrouei, D., Kefayat, A., Motaghi, H., Mehrgardi, M. A., & Javanmard, S. H. (2018). AS1411 aptamer conjugated gold nanoclusters as a targeted radiosensitizer for megavoltage radiation therapy of 4T1 breast cancer cells. RSC Advances, 8(8), 4249–4258. https://doi.org/10.1039/C7RA11116A
  • Ghochikyan, A. (2009). Rationale for peptide and DNA based epitope vaccines for Alzheimer's disease immunotherapy. CNS & Neurological Disorders Drug Targets, 8(2), 128–143. https://doi.org/10.2174/187152709787847298
  • Greenbaum, J., Sidney, J., Chung, J., Brander, C., Peters, B., & Sette, A. (2011). Functional classification of class II human leukocyte antigen (HLA) molecules reveals seven different supertypes and a surprising degree of repertoire sharing across supertypes. Immunogenetics, 63(6), 325–335. https://doi.org/10.1007/s00251-011-0513-0
  • Gu, Y., Sun, X., Li, B., Huang, J., Zhan, B., & Zhu, X. (2017). Vaccination with a paramyosin-based multi-epitope vaccine elicits significant protective immunity against Trichinella spiralis infection in mice. Frontiers in Microbiology, 8, 1475. https://doi.org/10.3389/fmicb.2017.01475
  • Guex, N., & Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis, 18(15), 2714–2723. https://doi.org/10.1002/elps.1150181505
  • Gul, H., Ali, S. S., Saleem, S., Khan, S., Khan, J., Wadood, A., Rehman, A. U., Ullah, Z., Ali, S., Khan, H., Hussain, Z., Akbar, F., Khan, A., & Wei, D.-Q. (2020). Subtractive proteomics and immunoinformatics approaches to explore Bartonella bacilliformis proteome (virulence factors) to design B and T cell multi-epitope subunit vaccine. Infection, Genetics and Evolution : Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 85, 104551. https://doi.org/10.1016/j.meegid.2020.104551
  • Hakenberg, J., Nussbaum, A. K., Schild, H., Rammensee, H.-G., Kuttler, C., Holzhütter, H.-G., Kloetzel, P.-M., Kaufmann, S. H. E., & Mollenkopf, H.-J. (2003). MAPPP: MHC class I antigenic peptide processing prediction. Applied Bioinformatics, 2(3), 155–158.
  • Hattotuwagama, C. K., Guan, P., Doytchinova, I. A., Zygouri, C., & Flower, D. R. (2004). Quantitative online prediction of peptide binding to the major histocompatibility complex. Journal of Molecular Graphics & Modelling, 22(3), 195–207. https://doi.org/10.1016/S1093-3263(03)00160-8
  • Ikram, A. (2018). Exploring NS3/4A, NS5A and NS5B proteins to design conserved subunit multi-epitope vaccine against HCV utilizing immunoinformatics approaches. Scientific Reports, 8(1), 1–14. https://doi.org/10.1038/s41598-018-34254-5
  • Ivashkiv, L. B. J. (2018). IFNγ: Signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy. Nature Reviews Immunology, 18(9), 545–558. https://doi.org/10.1038/s41577-018-0029-z
  • Jensen, K. K., Andreatta, M., Marcatili, P., Buus, S., Greenbaum, J. A., Yan, Z., Sette, A., Peters, B., & Nielsen, M. (2018). Improved methods for predicting peptide binding affinity to MHC class II molecules. Immunology, 154(3), 394–406. https://doi.org/10.1111/imm.12889
  • Joosse, S. A., Müller, V., Steinbach, B., Pantel, K., & Schwarzenbach, H. (2014). Circulating cell-free cancer-testis MAGE-A RNA. British Journal of Cancer, 111(5), 909–917. https://doi.org/10.1038/bjc.2014.360
  • Jorgovanovic, D. (2020). Roles of IFN-γ in tumor progression and regression: A review. Biomarker Research, 8(1), 49. https://doi.org/10.1186/s40364-020-00228-x
  • Kagohara, L. T. (2019). Cancer/testis antigens differentially expressed in prostate cancer: Potential new biomarkers and targets for immunotherapies. bioRxiv, 646869.
  • Kao, D. J., & Hodges, R. S. (2009). Advantages of a synthetic peptide immunogen over a protein immunogen in the development of an anti-pilus vaccine for Pseudomonas aeruginosa. Chemical Biology & Drug Design, 74(1), 33–42. https://doi.org/10.1111/j.1747-0285.2009.00825.x
  • Kefayat, A. (2019). C-Phycocyanin: A natural product with radiosensitizing property for enhancement of colon cancer radiation therapy efficacy through inhibition of COX-2 expression. Scientific Reports, 9(1), 19161. https://doi.org/10.1038/s41598-019-55605-w
  • Keşmir, C., Nussbaum, A. K., Schild, H., Detours, V., & Brunak, S. (2002). Prediction of proteasome cleavage motifs by neural networks. Protein Engineering, 15(4), 287–296. https://doi.org/10.1093/protein/15.4.287
  • Khalili, S., Rahbar, M. R., Dezfulian, M. H., & Jahangiri, A. (2015). In silico analyses of Wilms׳ tumor protein to designing a novel multi-epitope DNA vaccine against cancer. Journal of Theoretical Biology, 379, 66–78. https://doi.org/10.1016/j.jtbi.2015.04.026
  • Khan, M., Khan, S., Ali, A., Akbar, H., Sayaf, A. M., Khan, A., & Wei, D.-Q. (2019). Immunoinformatics approaches to explore Helicobacter Pylori proteome (Virulence Factors) to design B and T cell multi-epitope subunit vaccine. Scientific Reports, 9(1), 1–13. https://doi.org/10.1038/s41598-019-49354-z
  • Kosaka-Suzuki, N., Suzuki, T., Pugacheva, E. M., Vostrov, A. A., Morse, H. C., Loukinov, D., & Lobanenkov, V. (2011). Transcription factor BORIS (Brother of the Regulator of Imprinted Sites) directly induces expression of a cancer-testis antigen, TSP50, through regulated binding of BORIS to the promoter. The Journal of Biological Chemistry, 286(31), 27378–27388. https://doi.org/10.1074/jbc.M111.243576
  • Kozak, M. (1987). An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Research, 15(20), 8125–8148. https://doi.org/10.1093/nar/15.20.8125
  • Kozakov, D., Beglov, D., Bohnuud, T., Mottarella, S. E., Xia, B., Hall, D. R., & Vajda, S. (2013). How good is automated protein docking? Proteins, 81(12), 2159–2166. https://doi.org/10.1002/prot.24403
  • Kozakov, D., Brenke, R., Comeau, S. R., & Vajda, S. (2006). PIPER: An FFT-based protein docking program with pairwise potentials. Proteins, 65(2), 392–406. https://doi.org/10.1002/prot.21117
  • Kozakov, D., Hall, D. R., Xia, B., Porter, K. A., Padhorny, D., Yueh, C., Beglov, D., & Vajda, S. (2017). The ClusPro web server for protein–protein docking. Nature Protocols, 12(2), 255–278. https://doi.org/10.1038/nprot.2016.169
  • Kringelum, J. V., Lundegaard, C., Lund, O., & Nielsen, M. (2012). Reliable B cell epitope predictions: Impacts of method development and improved benchmarking. PLoS Computational Biology, 8(12), e1002829. https://doi.org/10.1371/journal.pcbi.1002829
  • Kudrin, A. (2012). Overview of cancer vaccines: Considerations for development. Human Vaccines & Immunotherapeutics, 8(9), 1335–1353. https://doi.org/10.4161/hv.20518
  • Lang, K., Entschladen, F., Weidt, C., & Zaenker, K. S. (2006). Tumor immune escape mechanisms: Impact of the neuroendocrine system. Cancer Immunology, Immunotherapy: CII, 55(7), 749–760. https://doi.org/10.1007/s00262-006-0126-x
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
  • Leifert, J. A., Rodriguez-Carreno, M. P., Rodriguez, F., & Whitton, J. L. (2004). Targeting plasmid-encoded proteins to the antigen presentation pathways. Immunological Reviews, 199(1), 40–53. https://doi.org/10.1111/j.0105-2896.2004.0135.x
  • Li, Q.-X., Feuer, G., Ouyang, X., & An, X. (2017). Experimental animal modeling for immuno-oncology. Pharmacology & Therapeutics, 173, 34–46. https://doi.org/10.1016/j.pharmthera.2017.02.002
  • Li, W., Joshi, M. D., Singhania, S., Ramsey, K. H., & Murthy, A. K. (2014). Peptide vaccine: Progress and Challenges. Vaccines, 2(3), 515–536. https://doi.org/10.3390/vaccines2030515
  • Lindahl, E., Azuara, C., Koehl, P., & Delarue, M. (2006). NOMAD-Ref: Visualization, deformation and refinement of macromolecular structures based on all-atom normal mode analysis. Nucleic Acids Research, 34(Web Server issue), W52–W56. https://doi.org/10.1093/nar/gkl082
  • Livingston, B., Crimi, C., Newman, M., Higashimoto, Y., Appella, E., Sidney, J., & Sette, A. (2002). A rational strategy to design multiepitope immunogens based on multiple Th lymphocyte epitopes. Journal of Immunology (Baltimore, MD: 1950), 168(11), 5499–5506. https://doi.org/10.4049/jimmunol.168.11.5499
  • Lo, Y.-S., Lin, C.-Y., & Yang, J.-M. (2010). PCFamily: A web server for searching homologous protein complexes. Nucleic Acids Research, 38(Web Server issue), W516–W522. https://doi.org/10.1093/nar/gkq464
  • Lopes, A., Vandermeulen, G., & Préat, V. (2019). Cancer DNA vaccines: Current preclinical and clinical developments and future perspectives. Journal of Experimental & Clinical Cancer Research: CR, 38(1), 146. https://doi.org/10.1186/s13046-019-1154-7
  • Magnan, C. N., Randall, A., & Baldi, P. (2009). SOLpro: Accurate sequence-based prediction of protein solubility. Bioinformatics (Oxford, England), 25(17), 2200–2207. https://doi.org/10.1093/bioinformatics/btp386
  • Magnan, C. N., Zeller, M., Kayala, M. A., Vigil, A., Randall, A., Felgner, P. L., & Baldi, P. (2010). High-throughput prediction of protein antigenicity using protein microarray data. Bioinformatics (Oxford, England), 26(23), 2936–2943. https://doi.org/10.1093/bioinformatics/btq551
  • Maurer-Stroh, S., Krutz, N. L., Kern, P. S., Gunalan, V., Nguyen, M. N., Limviphuvadh, V., Eisenhaber, F., & Gerberick, G. F. (2019). AllerCatPro-prediction of protein allergenicity potential from the protein sequence. Bioinformatics (Oxford, England), 35(17), 3020–3027. https://doi.org/10.1093/bioinformatics/btz029
  • Mauro, V. P., & Chappell, S. A. (2014). A critical analysis of codon optimization in human therapeutics. Trends in Molecular Medicine, 20(11), 604–613. https://doi.org/10.1016/j.molmed.2014.09.003
  • Medina, D. J. E. (2005). Mammary developmental fate and breast cancer risk. Endocrine-Related Cancer, 12(3), 483–495. https://doi.org/10.1677/erc.1.00804
  • Meza, B., Ascencio, F., Sierra-Beltrán, A. P., Torres, J., & Angulo, C. (2017). A novel design of a multi-antigenic, multistage and multi-epitope vaccine against Helicobacter pylori: An in silico approach. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 49, 309–317. https://doi.org/10.1016/j.meegid.2017.02.007
  • Mitropoulos, V., Mütze, A., & Fischer, P. (2014). Mechanical properties of protein adsorption layers at the air/water and oil/water interface: A comparison in light of the thermodynamical stability of proteins. Advances in Colloid and Interface Science, 206, 195–206. https://doi.org/10.1016/j.cis.2013.11.004
  • Nazifi, N. (2019). In vivo immunogenicity assessment and vaccine efficacy evaluation of a chimeric tandem repeat of epitopic region of OMP31 antigen fused to interleukin 2 (IL-2) against Brucella melitensis in BALB/c mice. BMC Veterinary Research, 15(1), 402. https://doi.org/10.1186/s12917-019-2074-7
  • Nezafat, N., Ghasemi, Y., Javadi, G., Khoshnoud, M. J., & Omidinia, E. (2014). A novel multi-epitope peptide vaccine against cancer: An in silico approach. Journal of Theoretical Biology, 349, 121–134. https://doi.org/10.1016/j.jtbi.2014.01.018
  • Nezafat, N., Sadraeian, M., Rahbar, M. R., Khoshnoud, M. J., Mohkam, M., Gholami, A., Banihashemi, M., & Ghasemi, Y. (2015). Production of a novel multi-epitope peptide vaccine for cancer immunotherapy in TC-1 tumor-bearing mice. Biologicals: Journal of the International Association of Biological Standardization, 43(1), 11–17. https://doi.org/10.1016/j.biologicals.2014.11.001
  • Nielsen, M., & Lund, O. (2009). NN-align. An artificial neural network-based alignment algorithm for MHC Class II peptide binding prediction. 10(1), 296.
  • Nielsen, M., Lundegaard, C., & Lund, O. (2007). Prediction of MHC class II binding affinity using SMM-align, a novel stabilization matrix alignment method. BMC Bioinformatics, 8(1), 238. https://doi.org/10.1186/1471-2105-8-238
  • Norell, H., Poschke, I., Charo, J., Wei, W. Z., Erskine, C., Piechocki, M. P., Knutson, K. L., Bergh, J., Lidbrink, E., & Kiessling, R. (2010). Vaccination with a plasmid DNA encoding HER-2/neu together with low doses of GM-CSF and IL-2 in patients with metastatic breast carcinoma: A pilot clinical trial. Journal of Translational Medicine, 8, 53 https://doi.org/10.1186/1479-5876-8-53
  • Okabayashi, K., Fujita, T., Miyazaki, J., Okada, T., Iwata, T., Hirao, N., Noji, S., Tsukamoto, N., Goshima, N., Hasegawa, H., Takeuchi, H., Ueda, M., Kitagawa, Y., & Kawakami, Y. (2012). Cancer-testis antigen BORIS is a novel prognostic marker for patients with esophageal cancer. Cancer Science, 103(9), 1617–1624. https://doi.org/10.1111/j.1349-7006.2012.02355.x
  • Oloomi, M., Javadi, M., Asadi Karam, M. R., Khezerloo, J. K., Haghri, Z., & Bouzari, S. (2020). Protective multi-epitope candidate vaccine for urinary tract infection. Biotechnology Reports (Amsterdam, Netherlands), 28, e00564. https://doi.org/10.1016/j.btre.2020.e00564
  • Pandey, R. K., Bhatt, T. K., & Prajapati, V. K. (2018). Novel immunoinformatics approaches to design multi-epitope subunit vaccine for malaria by investigating anopheles salivary protein. Scientific Reports, 8(1), 1–11. https://doi.org/10.1038/s41598-018-19456-1
  • Parvizpour, S., Razmara, J., & Omidi, Y. (2018). Breast cancer vaccination comes to age: Impacts of bioinformatics. BioImpacts, 8(3), 223–235. https://doi.org/10.15171/bi.2018.25
  • Paul, S. (2016). TepiTool: A pipeline for computational prediction of T cell epitope candidates. Current Protocols in Immunology, 114(1), 18.19. 1–18.19. 24. https://doi.org/10.1002/cpim.12
  • Pierleoni, A., Martelli, P. L., Fariselli, P., & Casadio, R. (2006). BaCelLo: A balanced subcellular localization predictor. Bioinformatics (Oxford, England), 22(14), e408–e416. https://doi.org/10.1093/bioinformatics/btl222
  • Pierson, T. C. (2010). Modeling antibody-enhanced dengue virus infection and disease in mice: Protection or pathogenesis? Cell Host & Microbe, 7(2), 85–86. https://doi.org/10.1016/j.chom.2010.02.004
  • Poland, G. A., Kennedy, R. B., & Ovsyannikova, I. G. (2011). Vaccinomics and personalized vaccinology: Is science leading us toward a new path of directed vaccine development and discovery? PLoS Pathogens, 7(12), e1002344. https://doi.org/10.1371/journal.ppat.1002344
  • Ponomarenko, J., Bui, H.-H., Li, W., Fusseder, N., Bourne, P. E., Sette, A., & Peters, B. (2008). ElliPro: A new structure-based tool for the prediction of antibody epitopes. BMC Bioinformatics, 9(1), 514. https://doi.org/10.1186/1471-2105-9-514
  • Rad, H. S., Mousavi, S. L., Rasooli, I., Amani, J., & Nadooshan, M. R. J. (2013). EspA-Intimin chimeric protein, a candidate vaccine against Escherichia coli O157:H7. Iranian Journal of Microbiology, 5(3), 244–251.
  • Radivojac, P., Vacic, V., Haynes, C., Cocklin, R. R., Mohan, A., Heyen, J. W., Goebl, M. G., & Iakoucheva, L. M. (2010). Identification, analysis, and prediction of protein ubiquitination sites. Proteins, 78(2), 365–380. https://doi.org/10.1002/prot.22555
  • Rodriguez, F., An, L. L., Harkins, S., Zhang, J., Yokoyama, M., Widera, G., Fuller, J. T., Kincaid, C., Campbell, I. L., & Whitton, J. L. (1998). DNA immunization with minigenes: Low frequency of memory cytotoxic T lymphocytes and inefficient antiviral protection are rectified by ubiquitination. Journal of Virology, 72(6), 5174–5181. https://doi.org/10.1128/JVI.72.6.5174-5181.1998
  • Rosa, D. S., Ribeiro, S. P., & Cunha-Neto, E. J. (2010). CD4+ T cell epitope discovery and rational vaccine design. Archivum Immunologiae et Therapiae Experimentalis, 58(2), 121–130. https://doi.org/10.1007/s00005-010-0067-0
  • Saadi, M., Karkhah, A., & Nouri, H. R. (2017). Development of a multi-epitope peptide vaccine inducing robust T cell responses against brucellosis using immunoinformatics based approaches. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 51, 227–234. https://doi.org/10.1016/j.meegid.2017.04.009
  • Safavi, A., et al. (2021). Efficacy of co-immunization with the DNA and peptide vaccines containing SYCP1 and ACRBP epitopes in a murine triple-negative breast cancer model. Human Vaccines and Immunotherapeutics, 17(1), 22-34. https://doi.org/10.1080/21645515.2020.1763693
  • Safavi, A., Kefayat, A., Abiri, A., Mahdevar, E., Behnia, A. H., & Ghahremani, F. (2019). In silico analysis of transmembrane protein 31 (TMEM31) antigen to design novel multiepitope peptide and DNA cancer vaccines against melanoma. Molecular Immunology, 112, 93–102. https://doi.org/10.1016/j.molimm.2019.04.030
  • Safavi, A., Kefayat, A., Ghahremani, F., Mahdevar, E., & Moshtaghian, J. (2019). Immunization using male germ cells and gametes as rich sources of cancer/testis antigens for inhibition of 4T1 breast tumors' growth and metastasis in BALB/c mice. International Immunopharmacology, 74, 105719. https://doi.org/10.1016/j.intimp.2019.105719
  • Safavi, A., Kefayat, A., Mahdevar, E., Abiri, A., & Ghahremani, F. (2020). Exploring the out of sight antigens of SARS-CoV-2 to design a candidate multi-epitope vaccine by utilizing immunoinformatics approaches. Vaccine, 38(48), 7612–7628. https://doi.org/10.1016/j.vaccine.2020.10.016
  • Safavi, A., Kefayat, A., Sotoodehnejadnematalahi, F., Salehi, M., & Modarressi, M. H. (2019a). In silico analysis of synaptonemal complex protein 1 (SYCP1) and acrosin binding protein (ACRBP) antigens to design novel multiepitope peptide cancer vaccine against breast cancer. International Journal of Peptide Research and Therapeutics, 25(4), 1343–1359. https://doi.org/10.1007/s10989-018-9780-z
  • Safavi, A., Kefayat, A., Sotoodehnejadnematalahi, F., Salehi, M., & Modarressi, M. H. (2019b). Production, purification, and in vivo evaluation of a novel multiepitope peptide vaccine consisted of immunodominant epitopes of SYCP1 and ACRBP antigens as a prophylactic melanoma vaccine. International Immunopharmacology, 76, 105872. https://doi.org/10.1016/j.intimp.2019.105872
  • Saha, S., & Raghava, G. P. S. (2004). BcePred: Prediction of Continuous B-Cell Epitopes in Antigenic Sequences Using Physico-Chemical Properties. International Conference on Artificial Immune Systems. Springer.
  • Saha, S., & Raghava, G. P. S. (2006). Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins, 65(1), 40–48. https://doi.org/10.1002/prot.21078
  • Schiller, J. T., & Lowy, D. R. (2010). Vaccines to prevent infections by oncoviruses. Annual Review of Microbiology, 64, 23–41. https://doi.org/10.1146/annurev.micro.112408.134019
  • Schrodinger, L. (2010). The PyMOL molecular graphics system. Version, 1(5).
  • Shan, D., Press, O. W., Tsu, T. T., Hayden, M. S., & Ledbetter, J. A. (1999). Characterization of scFv-Ig constructs generated from the anti-CD20 mAb 1F5 using linker peptides of varying lengths. Journal of Immunology (Baltimore, MD: 1950), 162(11), 6589–6595.
  • Sharma, G. N., Dave, R., Sanadya, J., Sharma, P., & Sharma, K. K. (2010). Various types and management of breast cancer: An overview. Journal of Advanced Pharmaceutical Technology & Research, 1(2), 109–126.
  • Shey, R. A. (2019). In-silico design of a multi-epitope vaccine candidate against onchocerciasis and related filarial diseases. Scientific Reports, 9(1), 4409. https://doi.org/10.1038/s41598-019-40833-x
  • Skwarczynski, M., & Toth, I. (2016). Peptide-based synthetic vaccines. Chemical Science, 7(2), 842–854. https://doi.org/10.1039/c5sc03892h
  • Snapper, C. M. (2018). Distinct immunologic properties of soluble versus particulate antigens. Frontiers in Immunology, 9.  https://doi.org/10.3389/fimmu.2018.00598
  • Soltanian, S., & Dehghani, H. (2018). BORIS: A key regulator of cancer stemness. Cancer Cell International, 18(1), 1–13. https://doi.org/10.1186/s12935-018-0650-8
  • Stanculeanu, D. L., Daniela, Z., Lazescu, A., Bunghez, R., & Anghel, R. (2016). Development of new immunotherapy treatments in different cancer types. Journal of Medicine and Life, 9(3), 240–248.
  • Steentoft, C., Vakhrushev, S. Y., Joshi, H. J., Kong, Y., Vester-Christensen, M. B., Schjoldager, K. T.-B G., Lavrsen, K., Dabelsteen, S., Pedersen, N. B., Marcos-Silva, L., Gupta, R., Bennett, E. P., Mandel, U., Brunak, S., Wandall, H. H., Levery, S. B., & Clausen, H. (2013). Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology . The EMBO Journal, 32(10), 1478–1488. https://doi.org/10.1038/emboj.2013.79
  • Steer, A. C. (2009). Group A Streptococcal vaccines: Facts versus fantasy. Current Opinion in Infectious Diseases, 22(6), 544–552. https://doi.org/10.1097/QCO.0b013e328332bbfe
  • Stranzl, T., Larsen, M. V., Lundegaard, C., & Nielsen, M. (2010). NetCTLpan: Pan-specific MHC class I pathway epitope predictions. Immunogenetics, 62(6), 357–368. https://doi.org/10.1007/s00251-010-0441-4
  • Suryanarayana, N. (2016). Soluble expression and characterization of biologically active bacillus anthracis protective antigen in Escherichia coli. Molecular Biology International, 2016(1), 1-11. https://doi.org/10.1155/2016/4732791
  • Tang, C.-T., Li, P.-C., Liu, I.-J., Liao, M.-Y., Chiu, C.-Y., Chao, D.-Y., & Wu, H.-C. (2015). An epitope-substituted DNA vaccine improves safety and immunogenicity against dengue virus type 2. PLoS Neglected Tropical Diseases, 9(7), e0003903. https://doi.org/10.1371/journal.pntd.0003903
  • Thiery, J. P., Acloque, H., Huang, R. Y. J., & Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell, 139(5), 871–890. https://doi.org/10.1016/j.cell.2009.11.007
  • Tiriveedhi, V. (2013). Mammaglobin-A cDNA vaccination of breast cancer patients induces antigen-specific cytotoxic CD4+ ICOS Hi T cells. Breast Cancer Research and Treatment, 138(1), 109–118. https://doi.org/10.1007/s10549-012-2110-9
  • Tomczak, K., Czerwińska, P., & Wiznerowicz, M. (2015). The Cancer Genome Atlas (TCGA): An immeasurable source of knowledge. Contemporary Oncology (Pozn), 19(1A), A68–A77. https://doi.org/10.5114/wo.2014.47136
  • Vazquez, E., Corchero, J. L., & Villaverde, A. J. (2011). Post-production protein stability: Trouble beyond the cell factory. Microbial Cell Factories, 10, 60. https://doi.org/10.1186/1475-2859-10-60
  • Vita, R., Zarebski, L., Greenbaum, J. A., Emami, H., Hoof, I., Salimi, N., Damle, R., Sette, A., & Peters, B. (2010). The immune epitope database 2.0. Nucleic Acids Research, 38(Database issue), D854–D862. https://doi.org/10.1093/nar/gkp1004
  • Weber, J. S. (1999). A phase I trial of an HLA-A1 restricted MAGE-3 epitope peptide with incomplete Freund's adjuvant in patients with resected high-risk melanoma. Journal of Immunotherapy, 22(5), 431–440.
  • Wei, W.-Z., Jones, R. F., Juhasz, C., Gibson, H., & Veenstra, J. (2015). Evolution of animal models in cancer vaccine development. Vaccine, 33(51), 7401–7407. https://doi.org/10.1016/j.vaccine.2015.07.075
  • Wiederstein, M., & Sippl, M. J. (2007). ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research, 35(Web Server issue), W407–W410. https://doi.org/10.1093/nar/gkm290
  • Zarling, A. L., Ficarro, S. B., White, F. M., Shabanowitz, J., Hunt, D. F., & Engelhard, V. H. (2000). Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. The Journal of Experimental Medicine, 192(12), 1755–1762. https://doi.org/10.1084/jem.192.12.1755
  • Zhang, L., Huang, Y., Lindstrom, A. R., Lin, T.-Y., Lam, K. S., & Li, Y. (2019). Peptide-based materials for cancer immunotherapy. Theranostics, 9(25), 7807–7825. https://doi.org/10.7150/thno.37194
  • Zhang, Y., Fang, M., Song, Y., Ren, J., Fang, J., & Wang, X. (2017). Brother of Regulator of Imprinted Sites (BORIS) suppresses apoptosis in colorectal cancer. Scientific Reports, 7(1), 40786–40712. https://doi.org/10.1038/srep40786
  • Zhou, W.-Y., Shi, Y., Wu, C., Zhang, W.-J., Mao, X.-H., Guo, G., Li, H.-X., & Zou, Q.-M. (2009). Therapeutic efficacy of a multi-epitope vaccine against Helicobacter pylori infection in BALB/c mice model. Vaccine, 27(36), 5013–5019. https://doi.org/10.1016/j.vaccine.2009.05.009

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.