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Research Article

In silico design of a trivalent multi-epitope global-coverage vaccine-candidate protein against influenza viruses: evaluation by molecular dynamics and immune system simulation

, , , &
Received 01 Feb 2023, Accepted 24 Nov 2023, Published online: 13 Dec 2023

References

  • Adam, K. M. (2021). Immunoinformatics approach for multi-epitope vaccine design against structural proteins and ORF1a polyprotein of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). Tropical Diseases, Travel Medicine and Vaccines, 7(1), 22. https://doi.org/10.1186/s40794-021-00147-1
  • Asthagiri Arunkumar, G., Ioannou, A., Wohlbold, T. J., Meade, P., Aslam, S., Amanat, F., Ayllon, J., García-Sastre, A., & Krammer, F. (2019). Broadly cross-reactive, nonneutralizing antibodies against influenza B virus hemagglutinin demonstrate effector function-dependent protection against lethal viral challenge in mice. Journal of Virology, 93(6), e01696–18. https://doi.org/10.1128/JVI.01696-18
  • Baloch, Z., Ikram, A., Shamim, S., Obaid, A., Awan, F. M., Naz, A., Rauff, B., Gilani, K., & Qureshi, J. A. (2022). Human coronavirus spike protein based multi-epitope vaccine against COVID-19 and potential future zoonotic coronaviruses by using immunoinformatic approaches. Vaccines, 10(7), 1150–1161. https://doi.org/10.3390/vaccines10071150
  • Bao, Y., Bolotov, P., Dernovoy, D., Kiryutin, B., Zaslavsky, L., Tatusova, T., Ostell, J., & Lipman, D. (2008). The influenza virus resource at the National Center for Biotechnology Information. Journal of Virology, 82(2), 596–601. https://doi.org/10.1128/JVI.02005-07
  • Bazhan, S. I., Antonets, D. V., Starostina, E. V., Ilyicheva, T. N., Kaplina, O. N., Marchenko, V. Y., Volkova, O. Y., Bakulina, A. Y., & Karpenko, L. I. (2022). In silico design of influenza a virus artificial epitope-based T-cell antigens and the evaluation of their immunogenicity in mice. Journal of Biomolecular Structure & Dynamics, 40(7), 3196–3212. https://doi.org/10.1080/07391102.2020.1845978
  • Bhattacharya, A., Tejero, R., & Montelione, G. T. (2007). Evaluating protein structures determined by structural genomics consortia. Proteins, 66(4), 778–795. https://doi.org/10.1002/prot.21165
  • Biere, B., Bauer, B., & Schweiger, B. (2010). Differentiation of influenza B virus lineages Yamagata and Victoria by real-time PCR. Journal of Clinical Microbiology, 48(4), 1425–1427. https://doi.org/10.1128/JCM.02116-09
  • 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
  • Choe, J., Kelker, M. S., & Wilson, I. A. (2005). Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science (New York, N.Y.), 309(5734), 581–585. https://doi.org/10.1126/science.1115253
  • Choo, J. A., Thong, S. Y., Yap, J., van Esch, W. J., Raida, M., Meijers, R., Lescar, J., Verhelst, S. H., & Grotenbreg, G. M. (2014). Bioorthogonal cleavage and exchange of major histocompatibility complex ligands by employing azobenzene‐containing peptides. Angewandte Chemie (International ed. in English), 53(49), 13390–13394. https://doi.org/10.1002/anie.201406295
  • Coughlan, L., & Palese, P. (2018). Overcoming barriers in the path to a universal influenza virus vaccine. Cell Host & Microbe, 24(1), 18–24. https://doi.org/10.1016/j.chom.2018.06.016
  • De Groot, A. S., Moise, L., Terry, F., Gutierrez, A. H., Hindocha, P., Richard, G., Hoft, D. F., Ross, T. M., Noe, A. R., Takahashi, Y., Kotraiah, V., Silk, S. E., Nielsen, C. M., Minassian, A. M., Ashfield, R., Ardito, M., Draper, S. J., & Martin, W. D. (2020). Better epitope discovery, precision immune engineering, and accelerated vaccine design using immunoinformatics tools. Frontiers in Immunology, 11, 442. https://doi.org/10.3389/fimmu.2020.00442
  • Dey, J., Mahapatra, S. R., Lata, S., Patro, S., Misra, N., & Suar, M. (2022a). Exploring Klebsiella pneumoniae capsule polysaccharide proteins to design multiepitope subunit vaccine to fight against pneumonia. Expert Review of Vaccines, 21(4), 569–587. https://doi.org/10.1080/14760584.2022.2021882
  • Dey, J., Mahapatra, S. R., Raj, T. K., Kaur, T., Jain, P., Tiwari, A., Patro, S., Misra, N., & Suar, M. (2022b). Designing a novel multi-epitope vaccine to evoke a robust immune response against pathogenic multidrug-resistant Enterococcus faecium bacterium. Gut Pathogens, 14(1), 21. https://doi.org/10.1186/s13099-022-00495-z
  • Doytchinova, I. A., & Flower, D. R. (2007a). Identifying candidate subunit vaccines using an alignment-independent method based on principal amino acid properties. Vaccine, 25(5), 856–866. https://doi.org/10.1016/j.vaccine.2006.09.032
  • Doytchinova, I. A., & Flower, D. R. (2007b). VaxiJen: A server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics, 8(1), 1–7. https://doi.org/10.1186/1471-2105-8-4
  • Doytchinova, I. A., & Flower, D. R. (2008). Bioinformatic approach for identifying parasite and fungal candidate subunit vaccines. Open Vaccine J, 1(1), 4.
  • Farahmand, B., Taheri, N., Shokouhi, H., Soleimanjahi, H., & Fotouhi, F. (2019). Chimeric protein consisting of 3M2e and HSP as a universal influenza vaccine candidate: From in silico analysis to preliminary evaluation. Virus Genes, 55(1), 22–32.
  • Galperin, M., Farenc, C., Mukhopadhyay, M., Jayasinghe, D., Decroos, A., Benati, D., Tan, L. L., Ciacchi, L., Reid, H. H., Rossjohn, J., Chakrabarti, L. A., & Gras, S. (2018). CD4+ T cell–mediated HLA class II cross-restriction in HIV controllers. Science Immunology, 3(24), eaat0687. https://doi.org/10.1126/sciimmunol.aat0687
  • Ghafoor, D., Zeb, A., Ali, S. S., Ali, M., Akbar, F., Ud Din, Z., Ur Rehman, S., Suleman, M., & Khan, W. (2023). Immunoinformatic based designing of potential immunogenic novel mRNA and peptide-based prophylactic vaccines against H5N1 and H7N9 avian influenza viruses. Journal of Biomolecular Structure & Dynamics. https://doi.org/10.1080/07391102.2023.2214228
  • Ghahremanifard, P., Afzali, F., Rostami, A., Nayeri, Z., Bambai, B., & Minuchehr, Z. (2020). Designing a novel multi-epitope T vaccine for “targeting protein for Xklp 2”(TPX2) in hepatocellular carcinoma based on immunoinformatics approach. International Journal of Peptide Research and Therapeutics, 26(2), 1127–1136. https://doi.org/10.1007/s10989-019-09915-2
  • Ghaznavi, H., Shirvaliloo, M., Sargazi, S., Mohammadghasemipour, Z., Shams, Z., Hesari, Z., Shahraki, O., Nazarlou, Z., Sheervalilou, R., & Shirvalilou, S. (2022). SARS‐ CoV‐ 2 and influenza viruses: Strategies to cope with coinfection and bioinformatics perspective. Cell Biology International, 46, 1009–1020. https://doi.org/10.1002/cbin.11800
  • Gholami, S., Mafakher, L., Fotouhi, F., Bambai, B., Cohan, R. A., Mehrbod, P., Shokouhi, H., & Farahmand, B. (2023). Computational peptide engineering approach for selection of the new C05 antibody-driven peptide with potency to blocking influenza a virus attachment; from in silico to in vivo. Journal of Biomolecular Structure & Dynamics. https://doi.org/10.1080/07391102.2023.2241554
  • Gras, S., Kedzierski, L., Valkenburg, S. A., Laurie, K., Liu, Y. C., Denholm, J. T., Richards, M. J., Rimmelzwaan, G. F., Kelso, A., Doherty, P. C., Turner, S. J., Rossjohn, J., & Kedzierska, K. (2010). Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proceedings of the National Academy of Sciences of the United States of America, 107(28), 12599–12604. https://doi.org/10.1073/pnas.1007270107
  • Grote, A., Hiller, K., Scheer, M., Münch, R., Nörtemann, B., Hempel, D. C., & Jahn, D. (2005). JCat: A novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Research, 33, W526–W531. https://doi.org/10.1093/nar/gki376
  • Gupta, S., Kapoor, P., Chaudhary, K., Gautam, A., Kumar, R., Raghava, G. P., & Open Source Drug Discovery Consortium. (2013). In silico approach for predicting toxicity of peptides and proteins. PLoS One, 8(9), e73957. https://doi.org/10.1371/journal.pone.0073957
  • Hasan, M., Ghosh, P. P., Azim, K. F., Mukta, S., Abir, R. A., Nahar, J., & Hasan Khan, M. M. (2019). Reverse vaccinology approach to design a novel multi-epitope subunit vaccine against avian influenza A (H7N9) virus. Microbial Pathogenesis, 130(5), 19–37. https://doi.org/10.1016/j.micpath.2019.02.023
  • Henry, C., Palm, A.-K E., Utset, H. A., Huang, M., Ho, I. Y., Zheng, N.-Y., Fitzgerald, T., Neu, K. E., Chen, Y.-Q., Krammer, F., Treanor, J. J., Sant, A. J., Topham, D. J., & Wilson, P. C. (2019). Monoclonal antibody responses after recombinant hemagglutinin vaccine versus subunit inactivated influenza virus vaccine: A comparative study. Journal of Virology, 93(21), e01150–19. https://doi.org/10.1128/JVI.01150-19
  • Ishida, H., Asami, J., Zhang, Z., Nishizawa, T., Shigematsu, H., Ohto, U., & Shimizu, T. (2021). Cryo-EM structures of Toll-like receptors in complex with UNC93B1. Nature Structural & Molecular Biology, 28(2), 173–180. https://doi.org/10.1038/s41594-020-00542-w
  • Jalalvand, A., Khatouni, S. B., Najafi, Z. B., Fatahinia, F., Ismailzadeh, N., & Farahmand, B. (2021). Computational drug repurposing study of antiviral drugs against main protease, RNA polymerase, and spike proteins of SARS-CoV-2 using molecular docking method. Journal of Basic and Clinical Physiology and Pharmacology, 33(1), 85–95. https://doi.org/10.1515/jbcpp-2020-0369
  • Keshavarz, M., Mirzaei, H., Salemi, M., Momeni, F., Mousavi, M. J., Sadeghalvad, M., Arjeini, Y., Solaymani-Mohammadi, F., Sadri Nahand, J., Namdari, H., Mokhtari-Azad, T., & Rezaei, F. (2019). Influenza vaccine: Where are we and where do we go? Reviews in Medical Virology, 29(1), e2014. https://doi.org/10.1002/rmv.2014
  • Lampejo, T. (2020). Influenza and antiviral resistance: An overview. European Journal of Clinical Microbiology & Infectious Diseases, 39(7), 1201–1208. https://doi.org/10.1007/s10096-020-03840-9
  • Li, H., Ding, J., & Chen, Y. (2003). Recombinant protein comprising multi-neutralizing epitopes induced high titer of antibodies against Influenza A virus. Immunobiology, 207(5), 305–313. https://doi.org/10.1078/0171-2985-00244
  • Liao, H. Y., Wang, S. C., Ko, Y. A., Lin, K. I., Ma, C., Cheng, T. J. R., & Wong, C. H. (2020). Chimeric hemagglutinin vaccine elicits broadly protective CD4 and CD8 T cell responses against multiple influenza strains and subtypes. Proceedings of the National Academy of Sciences, 117(30), 17757–17763. https://doi.org/10.1073/pnas.2004783117
  • Liu, W. J., Lan, J., Liu, K., Deng, Y., Yao, Y., Wu, S., Chen, H., Bao, L., Zhang, H., Zhao, M., Wang, Q., Han, L., Chai, Y., Qi, J., Zhao, J., Meng, S., Qin, C., Gao, G. F., & Tan, W. (2017). Protective T cell responses featured by concordant recognition of Middle East respiratory syndrome coronavirus–derived CD8+ T cell epitopes and host MHC. Journal of Immunology (Baltimore, MD.: 1950), 198(2), 873–882. https://doi.org/10.4049/jimmunol.1601542
  • 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
  • Mahapatra, S. R., Dey, J., Jaiswal, A., Roy, R., Misra, N., & Suar, M. (2022a). Immunoinformatics-guided designing of epitope-based subunit vaccine from Pilus assembly protein of Acinetobacter baumannii bacteria. Journal of Immunological Methods, 508, 113325. https://doi.org/10.1016/j.jim.2022.113325
  • Mahapatra, S. R., Dey, J., Raj, T. K., Kumar, V., Ghosh, M., Verma, K. K., Kaur, T., Kesawat, M. S., Misra, N., & Suar, M. (2022b). The potential of plant-derived secondary metabolites as novel drug candidates against Klebsiella pneumoniae: Molecular docking and simulation investigation. South African Journal of Botany, 149, 789–797. https://doi.org/10.1016/j.sajb.2022.04.043
  • Mahapatra, S. R., Dey, J., Raj, T. K., Misra, N., & Suar, M. (2023). Designing a next-generation multiepitope-based vaccine against Staphylococcus aureus using reverse vaccinology approaches. Pathogens (Basel, Switzerland), 12(3), 376. https://doi.org/10.3390/pathogens12030376
  • Maleki, A., Russo, G., Parasiliti Palumbo, G. A., & Pappalardo, F. (2021). In silico design of recombinant multi-epitope vaccine against influenza A virus. BMC Bioinformatics, 22(Suppl 14), 617. https://doi.org/10.1186/s12859-022-04581-6
  • 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
  • Mia, M. M., Hasan, M., Ahmed, S., & Rahman, M. N. (2022). Insight into the first multi-epitope-based peptide subunit vaccine against avian influenza A virus (H5N6): An immunoinformatics approach. Infection, Genetics and Evolution, 104, 105355. https://doi.org/10.1016/j.meegid.2022.105355
  • Narang, P. K., Dey, J., Mahapatra, S. R., Ghosh, M., Misra, N., Suar, M., Kumar, V., & Raina, V. (2021). Functional annotation and sequence-structure characterization of a hypothetical protein putatively involved in carotenoid biosynthesis in microalgae. South African Journal of Botany, 141, 219–226. https://doi.org/10.1016/j.sajb.2021.04.014
  • Narang, P. K., Dey, J., Mahapatra, S. R., Roy, R., Kushwaha, G. S., Misra, N., Suar, M., & Raina, V. (2022). Genome-based identification and comparative analysis of enzymes for carotenoid biosynthesis in microalgae. World Journal of Microbiology & Biotechnology, 38(1), 8. https://doi.org/10.1007/s11274-021-03188-y
  • Natarajan, K., McShan, A. C., Jiang, J., Kumirov, V. K., Wang, R., Zhao, H., Schuck, P., Tilahun, M. E., Boyd, L. F., Ying, J., Bax, A., Margulies, D. H., & Sgourakis, N. G. (2017). An allosteric site in the T-cell receptor Cβ domain plays a critical signalling role. Nature Communications, 8(1), 15260. https://doi.org/10.1038/ncomms15260
  • Nazeri, E., Farahmand, B., Fotouhi, F., Hashemi, M., Taheri, N., Shokohi, H., & Hatami, S. (2018) In Silico Analysis and Expression of Influenza Virus 3M2e-HA2 Chimer Protein Fused to C-Terminal Domain of Leishmania major HSP70. Journal of Microbiology, 11(8), e13777. https://doi.org/10.5812/jjm.13777.
  • Petrova, V. N., & Russell, C. A. (2018). The evolution of seasonal influenza viruses. Nature Reviews. Microbiology, 16(1), 47–60. https://doi.org/10.1038/nrmicro.2017.118
  • Pleguezuelos, O., Robinson, S., Stoloff, G. A., & Caparrós-Wanderley, W. (2012). Synthetic Influenza vaccine (FLU-v) stimulates cell mediated immunity in a double-blind, randomised, placebo-controlled Phase I trial. Vaccine, 30(31), 4655–4660. https://doi.org/10.1016/j.vaccine.2012.04.089
  • 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
  • Pourjafar, M., Shirafkan, N., Bakhtiari, S., Afshar, S., Saidijam, M., Jalalvand, A., & Taherkhani, A. (2023). In silico and in vitro evaluation of selected herbal compounds as robust HER-2 inhibitors for effective treatment of breast cancer. Research Journal of Pharmacognosy, 10(3), 43–59.
  • Pourseif, M. M., Moghaddam, G., Naghili, B., Saeedi, N., Parvizpour, S., Nematollahi, A., & Omidi, Y. (2018). A novel in silico minigene vaccine based on CD4+ T-helper and B-cell epitopes of EG95 isolates for vaccination against cystic echinococcosis. Computational Biology and Chemistry, 72, 150–163. https://doi.org/10.1016/j.compbiolchem.2017.11.008
  • Rapin, N., Lund, O., Bernaschi, M., & Castiglione, F. (2010). Computational immunology meets bioinformatics: The use of prediction tools for molecular binding in the simulation of the immune system. PLoS One, 5(4), e9862. https://doi.org/10.1371/journal.pone.0009862
  • Raymond, D. D., Bajic, G., Ferdman, J., Suphaphiphat, P., Settembre, E. C., Moody, M. A., Schmidt, A. G., & Harrison, S. C. (2018). Conserved epitope on influenza-virus hemagglutinin head defined by a vaccine-induced antibody. Proceedings of the National Academy of Sciences of the United States of America, 115(1), 168–173. https://doi.org/10.1073/pnas.1715471115
  • Reddy Chichili, V. P., Kumar, V., & Sivaraman, J. (2013). Linkers in the structural biology of protein–protein interactions. Protein Science, 22(2), 153–167. https://doi.org/10.1002/pro.2206
  • Sahoo, P., Dey, J., Mahapatra, S. R., Ghosh, A., Jaiswal, A., Padhi, S., Prabhuswamimath, S. C., Misra, N., & Suar, M. (2022). Nanotechnology and COVID-19 convergence: Toward new planetary health interventions against the pandemic. Omics, 26(9), 473–488. https://doi.org/10.1089/omi.2022.0072
  • Samji, T. (2009). Influenza A: Understanding the viral life cycle. The Yale Journal of Biology and Medicine, 82(4), 153–159.
  • Scott, C. A., Peterson, P. A., Teyton, L., & Wilson, I. A. (1998). Crystal structures of two I-Ad–peptide complexes reveal that high affinity can be achieved without large anchor residues. Immunity, 8(3), 319–329. https://doi.org/10.1016/s1074-7613(00)80537-3
  • Sharma, S., Kumari, V., Kumbhar, B. V., Mukherjee, A., Pandey, R., & Kondabagil, K. (2021). Immunoinformatics approach for a novel multi-epitope subunit vaccine design against various subtypes of Influenza A virus. Immunobiology, 226(2), 152053. https://doi.org/10.1016/j.imbio.2021.152053
  • Short, K. R., Kroeze, E. J. V., Fouchier, R. A., & Kuiken, T. (2014). Pathogenesis of influenza-induced acute respiratory distress syndrome. The Lancet Infectious Diseases, 14(1), 57–69. https://doi.org/10.1016/S1473-3099(13)70286-X
  • Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7(1), 539. https://doi.org/10.1038/msb.2011.75
  • Sippl, M. J. (1993). Recognition of errors in three‐dimensional structures of proteins. Proteins, 17(4), 355–362. https://doi.org/10.1002/prot.340170404
  • Sparrow, E., Wood, J. G., Chadwick, C., Newall, A. T., Torvaldsen, S., Moen, A., & Torelli, G. (2021). Global production capacity of seasonal and pandemic influenza vaccines in 2019. Vaccine, 39(3), 512–520. https://doi.org/10.1016/j.vaccine.2020.12.018
  • Sudeshna Panda, S., Dey, J., Mahapatra, S. R., Kushwaha, G. S., Misra, N., Suar, M., & Ghosh, M. (2022). Investigation on structural prediction of pectate lyase enzymes from different microbes and comparative docking studies with pectin: The economical waste from food industry. Geomicrobiology Journal, 39(3–5), 294–305. https://doi.org/10.1080/01490451.2021.1992042
  • Sun, W., Kirkpatrick, E., Ermler, M., Nachbagauer, R., Broecker, F., Krammer, F., & Palese, P. (2019). Development of influenza B universal vaccine candidates using the “mosaic” hemagglutinin approach. Journal of Virology, 93(12), 10–1128. https://doi.org/10.1128/JVI.00333-19
  • Tanji, H., Ohto, U., Shibata, T., Miyake, K., & Shimizu, T. (2013). Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science (New York, N.Y.), 339(6126), 1426–1429. https://doi.org/10.1126/science.1229159
  • Wang, D., Liu, D., Yuchi, J., He, F., Jiang, Y., Cai, S., Li, J., & Xu, D. (2020). MusiteDeep: A deep-learning based webserver for protein post-translational modification site prediction and visualization. Nucleic Acids Research, 48(W1), W140–W146. https://doi.org/10.1093/nar/gkaa275
  • 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, W407–W410. https://doi.org/10.1093/nar/gkm290
  • Yan, Y., Tao, H., He, J., & Huang, S. Y. (2020). The HDOCK server for integrated protein–protein docking. Nature Protocols, 15(5), 1829–1852. https://doi.org/10.1038/s41596-020-0312-x
  • Zhou, B., Lin, X., Wang, W., Halpin, R. A., Bera, J., Stockwell, T. B., Barr, I. G., & Wentworth, D. E. (2014). Universal influenza B virus genomic amplification facilitates sequencing, diagnostics, and reverse genetics. Journal of Clinical Microbiology, 52(5), 1330–1337. https://doi.org/10.1128/JCM.03265-13

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