Immunoinformatics analysis to design novel epitope based vaccine candidate targeting the glycoprotein and nucleoprotein of Lassa mammarenavirus (LASMV) using strains from Nigeria

References

• Abdellrazeq, G. S., Fry, L. M., Elnaggar, M. M., Bannantine, J. P., Schneider, D. A., Chamberlin, W. M., Mahmoud, A. H. A., Park, K.-T., Hulubei, V., & Davis, W. C. (2020). Simultaneous cognate epitope recognition by bovine CD4 and CD8 T cells is essential for primary expansion of antigen-specific cytotoxic T-cells following ex vivo stimulation with a candidate Mycobacterium avium subsp. Paratuberculosis peptide vaccine. Vaccine, 38(8), 2016–2025. https://doi.org/10.1016/j.vaccine.2019.12.052
   PubMed Web of Science ®Google Scholar
• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1-2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Adhikari, U. K., & Rahman, M. M. (2017). Overlapping CD8+ and CD4+ T-cell epitopes identification for the progression of epitope-based peptide vaccine from nucleocapsid and glycoprotein of emerging Rift Valley fever virus using immunoinformatics approach. Infection, Genetics and Evolution, 56, 75–91. https://doi.org/10.1016/j.meegid.2017.10.022
   PubMed Web of Science ®Google Scholar
• Almofti, Y. A., Abd-Elrahman, K. A., Gassmallah, S. A. E., & Salih, M. A. (2018). Multi epitopes vaccine prediction against severe acute respiratory syndrome (SARS) coronavirus using immunoinformatics approaches. American Journal of Microbiological Research, 6(3), 94–114. 10.12691/ajmr-6-3-5
   Google Scholar
• Al-Shura, A. N. (2020). Lymphocytes. In Advanced hematology in integrated cardiovascular Chinese medicine (pp. 41–46). Elsevier. 10.1016/978-0-12-817572-9.00007-0
   Google Scholar
• Altschul, S. F., Wootton, J. C., Michael Gertz, E., Agarwala, R., Morgulis, A., Schäffer, A. A., & Yu, Y.-K. (2005). Protein database searches using compositionally adjusted substitution matrices. The FEBS Journal, 272(20), 5101–5109. https://doi.org/10.1111/j.1742-4658.2005.04945.x
   PubMed Web of Science ®Google Scholar
• Andersen, K. G., Shapiro, B. J., Matranga, C. B., Sealfon, R., Lin, A. E., Moses, L. M., Folarin, O. A., Goba, A., Odia, I., Ehiane, P. E., Momoh, M., England, E. M., Winnicki, S., Branco, L. M., Gire, S. K., Phelan, E., Tariyal, R., Tewhey, R., Omoniwa, O., … Sabeti, P. C. (2015). Clinical sequencing uncovers origins and evolution of Lassa virus. Cell, 162(4), 738–750. https://doi.org/10.1016/j.cell.2015.07.020
   PubMed Web of Science ®Google Scholar
• Asogun, D. A., Adomeh, D. I., Ehimuan, J., Odia, I., Hass, M., Gabriel, M., Olschläger, S., Becker-Ziaja, B., Folarin, O., Phelan, E., Ehiane, P. E., Ifeh, V. E., Uyigue, E. A., Oladapo, Y. T., Muoebonam, E. B., Osunde, O., Dongo, A., Okokhere, P. O., Okogbenin, S. A., … Günther, S. (2012). Molecular diagnostics for lassa fever at Irrua specialist teaching hospital, Nigeria: Lessons learnt from two years of laboratory operation. PLoS Neglected Tropical Diseases, 6(9), e1839. https://doi.org/10.1371/journal.pntd.0001839
   PubMed Web of Science ®Google Scholar
• Atapour, A., Mokarram, P., MostafaviPour, Z., Hosseini, S. Y., Ghasemi, Y., Mohammadi, S., & Nezafat, N. (2019). Designing a fusion protein vaccine against HCV: An in silico approach. International Journal of Peptide Research and Therapeutics, 25(3), 861–872. https://doi.org/10.1007/s10989-018-9735-4
   Web of Science ®Google Scholar
• Benkert, P., Biasini, M., & Schwede, T. (2011). Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics, 27(3), 343–350. https://doi.org/10.1093/bioinformatics/btq662
   PubMed Web of Science ®Google Scholar
• Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2013). GenBank. Nucleic Acids Research, 41(Database issue), D36–D42. https://doi.org/10.1093/nar/gks1195
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• BIOVIA. (2015). Discovery studio modeling environment. Dassault Systemes, Release, 4.
   Google Scholar
• Boehme, K. W., & Compton, T. (2004). Innate sensing of viruses by toll-like receptors. Journal of Virology, 78(15), 7867–7873. https://doi.org/10.1128/JVI.78.15.7867-7873.2004
   PubMed Web of Science ®Google Scholar
• Bonner, P. C., Schmidt, W. P., Belmain, S. R., Oshin, B., Baglole, D., & Borchert, M. (2007). Poor housing quality increases risk of rodent infestation and Lassa fever in refugee camps of Sierra Leone. The American Journal of Tropical Medicine and Hygiene, 77(1), 169–175.
   PubMed Web of Science ®Google Scholar
• Borthwick, N., Silva-Arrieta, S., Llano, A., Takiguchi, M., Brander, C., & Hanke, T. (2020). Novel nested peptide epitopes recognized by CD4+ T cells induced by HIV-1 conserved-region vaccines. Vaccines, 8(1), 28. https://doi.org/10.3390/vaccines8010028
   Web of Science ®Google Scholar
• Bowie, J. U., Luthy, R., & Eisenberg, D. (1991). A method to identify protein sequences that fold into a known three-dimensional structure. Science, 253(5016), 164–170. https://doi.org/10.1126/science.1853201
   PubMed Web of Science ®Google Scholar
• Brancatisano, F., Maisetta, G., Barsotti, F., Esin, S., Miceli, M., Gabriele, M., Giuca, M. R., Campa, M., & Batoni, P. (2011). Reduced human beta defensin 3 in individuals with periodontal disease. Journal of Dental Research, 90(2), 241–245. https://doi.org/10.1177/0022034510385686
   PubMed Web of Science ®Google Scholar
• Buchan, D. W. A., & Jones, D. T. (2019). The PSIPRED protein analysis workbench: 20 years on. Nucleic Acids Research, 47(W1), W402–W407. https://doi.org/10.1093/nar/gkz297
   PubMed Web of Science ®Google Scholar
• Bui, H., John, S., Wei, L., Nicolas, F., & Alessandro, S. (2007). Development of an epitope conservancy analysis tool to facilitate the design of epitope-based diagnostics and vaccines. BMC Bioinformatics, 8, 361. https://doi.org/10.1186/1471-2105-8-361
   PubMed Web of Science ®Google Scholar
• Bunkute, E., Cummins, C., Crofts, F. J., Bunce, G., Nabney, I. T., & Flower, D. R. (2015). PIP-DB: The Protein Isoelectric Point database. Bioinformatics, 31(2), 295–296. https://doi.org/10.1093/bioinformatics/btu637
   PubMed Web of Science ®Google Scholar
• Calis, J. J., Maybeno, M., Greenbaum, J. A., Weiskopf, D., De Silva, A. D., Sette, A., Keşmir, C., & Peters, B. (2013). Properties of MHC class I presented peptides that enhance immunogenicity. PLoS Computational Biology, 9(10), e1003266. https://doi.org/10.1371/journal.pcbi.1003266
   PubMed Web of Science ®Google Scholar
• Carvalho, L. H., Sano, G. I., Hafalla, J. C., Morrot, A., De Lafaille, M. A. C., & Zavala, F. (2002). IL-4-secreting CD4+ T cells are crucial to the development of CD8+ T-cell responses against malaria liver stages. Nature Medicine, 8(2), 166–170. https://doi.org/10.1038/nm0202-166
   PubMed Web of Science ®Google Scholar
• Castiglione, F., Mantile, F., De Berardinis, P., & Prisco, A. (2012). How the interval between prime and boost injection affects the immune response in a computational model of the immune system. Computational and Mathematical Methods in Medicine, 2012, 1–9. https://doi.org/10.1155/2012/842329
   Web of Science ®Google Scholar
• Channappanavar, R., & Perlman, S. (2020). Evaluation of activation and inflammatory activity of myeloid cells during pathogenic human coronavirus infection. In R. Vijay (Ed.), MERS coronavirus: Methods and protocols (pp. 195–204). Springer US.
   Google Scholar
• Charrel, R. N., & De Lamballerie, X. (2003). Arenaviruses other than Lassa virus. Antiviral Research, 57(1-2), 89–100. https://doi.org/10.1016/S0166-3542(02)00202-4
   PubMed Web of Science ®Google Scholar
• Chatterjee, N., Ojha, R., Khatoon, N., & Prajapati, V. K. (2018). Scrutinizing Mycobacterium tuberculosis membrane and secretory proteins to formulate multiepitope subunit vaccine against pulmonary tuberculosis by utilizing immunoinformatic approaches. International Journal of Biological Macromolecules, 118(Pt A), 180–188. https://doi.org/10.1016/j.ijbiomac.2018.06.080
   PubMedGoogle Scholar
• Chauhan, V., Rungta, T., Goyal, K., & Singh, M. P. (2019). Designing a multi-epitope based vaccine to combat Kaposi Sarcoma utilizing immunoinformatics approach. Scientific Reports, 9(1), 2517. https://doi.org/10.1038/s41598-019-39299-8
   PubMedGoogle Scholar
• Chen, R. (2012). Bacterial expression systems for recombinant protein production: E. coli and beyond. Biotechnology Advances, 30(5), 1102–1107. https://doi.org/10.1016/j.biotechadv.2011.09.013
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Chukwudozie, O. S., Gray, C. M., Fagbayi, T. A., Chukwuanukwu, R. C., Oyebanji, V. O., Bankole, T. T., Adewole, A. R., & Daniel, E. M. (2020). Immuno-informatics design of a multimeric epitope peptide based vaccine targeting SARS-CoV-2 spike glycoprotein. bioRxiv preprint. https://doi.org/10.1101/2020.07.30.228221. this version posted July 30, 2020.
   Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Craig, D. B., & Dombkowski, A. A. (2013). Disulfide by Design 2.0: A web-based tool for disulfide engineering in proteins. BMC Bioinformatics, 14, 346. https://doi.org/10.1186/1471-2105-14-346
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• de Oliveira, T. S. F., Passos, M. S., Kato, R., Salgado, Á., Xavier, J., Jaiswal, A. K., Soares, S. C., Azevedo, V., Giovanetti, M., Tiwari, S., & Alcantara, L. C. J. (2020). Multi-epitope based vaccine against Yellow fever virus applying immunoinformatics approaches. Journal of Biomolecular Structure and Dynamics, 39, 1–17. https://doi.org/10.1080/07391102.2019.1707120
   Web of Science ®Google Scholar
• DeLano, W. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter on Protein Crystallography, 40(1), 82–92.
   Google Scholar
• Dey, A. K., Malyala, P., & Singh, M. (2014). Physicochemical and functional characterization of vaccine antigens and adjuvants. Expert Review of Vaccines, 13(5), 671–685. https://doi.org/10.1586/14760584.2014.907528
   PubMed Web of Science ®Google Scholar
• Dhanda, S. K., Gupta, S., Vir, P., & Raghava, G. P. (2013). Prediction of IL4 inducing peptides. Clinical & Developmental Immunology, 2013, 263952. https://doi.org/10.1155/2013/263952
   PubMedGoogle Scholar
• Dhanda, S. K., Vir, P., & Raghava, G. P. (2013). Designing of interferon-gamma inducing MHC class-II binders. Biology Direct, 8, 30. https://doi.org/10.1186/1745-6150-8-30
   PubMed Web of Science ®Google Scholar
• Dong, Q., Zhou, S., & Guan, J. (2009). A new taxonomy-based protein fold recognition approach based on autocross-covariance transformation. Bioinformatics, 25(20), 2655–2662. https://doi.org/10.1093/bioinformatics/btp500
   PubMed Web of Science ®Google Scholar
• Dimitrov, I., Flower, D. R., & Doytchinova, I. (2013). AllerTOP – A server for in silico prediction of allergens. BMC Bioinformatics, 14(Suppl 6), S4. https://doi.org/10.1186/1471-2105-14-S6-S4
   PubMed Web of Science ®Google Scholar
• Dorosti, H., Eslami, M., Negahdaripour, M., Ghoshoon, M. B., Gholami, A., Heidari, R., Dehshahri, A., Erfani, N., Nezafat, N., & Ghasemi, Y. (2019). Vaccinomics approach for developing multi-epitope peptide pneumococcal vaccine. Journal of Biomolecular Structure & Dynamics, 37(13), 3524–3535. https://doi.org/10.1080/07391102.2018.1519460
   PubMed Web of Science ®Google Scholar
• Doytchinova, I. A., & Flower, D. R. (2007). VaxiJen: A server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics, 8(1), 4. https://doi.org/10.1186/1471-2105-8-4
   PubMed Web of Science ®Google Scholar
• Duhovny, D., Nussinov, R., & Wolfson, H. J. (2002). Efficient unbound docking of rigid molecules. In International workshop on algorithms in bioinformatics (pp. 185–200). Springer.
   Google Scholar
• Ehichioya, D. U., Dellicour, S., Pahlmann, M., Rieger, T., Oestereich, L., Becker-Ziaja, B., Cadar, D., Ighodalo, Y., Olokor, T., Omomoh, E., Oyakhilome, J., Omiunu, R., Agbukor, J., Ebo, B., Aiyepada, J., Ebhodaghe, P., Osiemi, B., Ehikhametalor, S., Akhilomen, P., … Günther, S. (2019). Phylogeography of Lassa virus in Nigeria. Journal of Virology, 93(21), e00929-19. https://doi.org/10.1128/JVI.00929-19
   PubMed Web of Science ®Google Scholar
• 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 J. M. Walker (Ed.), The proteomics protocols handbook (pp. 571–607). Humana Press.
   Google Scholar
• Goerdt, S., & Orfanos, C. E. (1999). Other functions, other genes: Alternative activation of antigen-presenting cells. Immunity, 10(2), 137–142. https://doi.org/10.1016/S1074-7613(00)80014-X
   PubMed Web of Science ®Google Scholar
• Goldberg, M. F., Roeske, E. K., Ward, L. N., Pengo, T., Dileepan, T., Kotov, D. I., & Jenkins, M. K. (2018). Salmonella persist in activated macrophages in T cell-sparse granulomas but are contained by surrounding CXCR3 ligand-positioned Th1 cells. Immunity, 49(6), 1090–1102. https://doi.org/10.1016/j.immuni.2018.10.009
   PubMed Web of Science ®Google Scholar
• Gonzalez, J. P., Emonet, S., Lamballerie, X. D., & Charrel, R. A. (2007). In J. E. Childs, J. S. Mackenzie, & J. A. Richt (Eds.), Wildlife and emerging zoonotic diseases: The biology, circumstances and consequences of cross-species transmission (Vol. 315, pp. 253–288). Springer.
   Google Scholar
• Gori, A., Longhi, R., Peri, C., & Colombo, G. (2013). Peptides for immunological purposes: Design, strategies and applications. Amino Acids, 45(2), 257–268. https://doi.org/10.1007/s00726-013-1526-9
   PubMed Web of Science ®Google Scholar
• 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(2), 526–531. https://doi.org/10.1093/nar/gki376
   Google Scholar
• Gu, Y., Sun, X., Li, B., Huang, J., Zhan, B., & Zhu, X. (2017). Vaccination with a paramyosin-based multi-epitope vaccine elicits signifcant protective immunity against Trichinella spiralis infection in mice. Frontiers in Microbiology, 8, 1–9. https://doi.org/10.3389/fmicb.2017.01475
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Hallam, H. J., Hallam, S., Rodriguez, S. E., Barrett, A. D. T., Beasley, D. W. C., Chua, A., Ksiazek, T. G., Milligan, G. N., Sathiyamoorthy, V., & Reece, L. M. (2018). Baseline mapping of Lassa fever virology, epidemiology and vaccine research and development reviewarticle. NPJ Vaccines, 3(1), 3-11. https://doi.org/10.1038/s41541-018-0049-5
   Google Scholar
• Hamasaki-Katagiri, N., Lin, B. C., Simon, J., Hunt, R. C., Schiller, T., Russek-Cohen, E., Komar, A. A., Bar, H., & Kimchi-Sarfaty, C. (2017). The importance of mRNA structure in determining the pathogenicity of synonymous and non-synonymous mutations in haemophilia. Haemophilia, 23(1), e8–e17. https://doi.org/10.1111/hae.13107
   PubMed Web of Science ®Google Scholar
• Hastie, K. M., Kimberlin, C. R., Zandonatti, M. A., MacRae, I. J., & Saphire, E. O. (2011). Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3' to 5' exonuclease activity essential for immune suppression. Proceedings of the National Academy of Sciences of the United States of America, 108(6), 2396–2401. https://doi.org/10.1073/pnas.1016404108
   PubMed Web of Science ®Google Scholar
• Heinrich, M. L. (2020). Antibodies from Sierra Leone and Nigerian Lassa fever survivors cross-react with recombinant proteins representing Lassa viruses of divergent lineages. Nature Reports, 10, 16030.
   PubMed Web of Science ®Google Scholar
• Heo, L., Park, H., & Seok, C. (2013). GalaxyRefne: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41, 384–388. https://doi.org/10.1093/nar/gkt458
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A Linear Constraint Solver for Molecular Simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H.) https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
   Web of Science ®Google Scholar
• Hoque, M. N., Istiaq, A., Clement, R. A., Sultana, M., Crandall, K. A., Siddiki, A. Z., & Hossain, M. A. (2019). Metagenomic deep sequencing reveals association of microbiome signature with functional biases in bovine mastitis. Scientific Reports, 9(1), 1–14. https://doi.org/10.1038/s41598-019-49468-4
   PubMed Web of Science ®Google Scholar
• Ibukun, F. I. (2020). Inter-lineage variation of Lassa virus glycoprotein epitopes: A challenge to Lassa virus vaccine development. Viruses, 12(4), 386. https://doi.org/10.3390/v12040386
   PubMed Web of Science ®Google Scholar
• Jabbar, B., Rafique, S., Salo-Ahen, O. M. H., Ali, A., Munir, M., Idrees, M., Mirza, M. U., Vanmeert, M., Shah, S. Z., Jabbar, I., & Rana, M. A. (2018). Antigenic peptide prediction from E6 and E7 oncoproteins of HPV types 16 and 18 for therapeutic vaccine design using immunoinformatics and MD simulation analysis. Frontiers in Immunology, 9, 3000. https://doi.org/10.3389/fimmu.2018.03000
   PubMed Web of Science ®Google Scholar
• Jose, L. S., Marta, G., & Pedro, A. (2017). Peptide-based immunotherapeutics and vaccines 2017. Journal of Immunology Research, 2017, 34-48. https://doi.org/10.1155/2017/2680160
   Google Scholar
• Kafetzopoulou, L. E., Pullan, S. T., Lemey, P., Suchard, M. A., Ehichioya, D. U., Pahlmann, M., Thielebein, A., Hinzmann, J., Oestereich, L., Wozniak, D. M., Efthymiadis, K., Schachten, D., Koenig, F., Matjeschk, J., Lorenzen, S., Lumley, S., Ighodalo, Y., Adomeh, D. I., Olokor, T., … Duraffour, S. (2019). Metagenomic sequencing at the epicenter of the Nigeria 2018 Lassa fever outbreak. Science, 363(6422), 74–77. https://doi.org/10.1126/science.aau9343
   PubMed Web of Science ®Google Scholar
• Kalita, P., Lyngdoh, D. L., Padhi, A. K., Shukla, H., & Tripathi, T. (2019). Development of multi-epitope driven subunit vaccine against Fasciola gigantica using immunoinformatics approach. International Journal of Biological Macromolecules, 138, 224–233. https://doi.org/10.1016/j.ijbiomac.2019.07.024
   PubMed Web of Science ®Google Scholar
• Källberg, M., Wang, H., Wang, S., Peng, J., Wang, Z., Lu, H., & Xu, J. (2017). Template-based protein structure modeling using the RaptorX web server. Physiology & Behavior, 176(8), 139–148. https://doi.org/10.1016/j.physbeh.2017.03.040
   PubMedGoogle Scholar
• Kambayashi, T., & Laufer, T. M. (2014). Atypical MHC class II-expressing antigen-presenting cells: Can anything replace a dendritic cell? Nature Reviews. Immunology, 14(11), 719–730. https://doi.org/10.1038/nri3754
   PubMed Web of Science ®Google Scholar
• 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), 13321. https://doi.org/10.1038/s41598-019-49354-z
   PubMedGoogle Scholar
• Khatoon, N., Pandey, R. K., & Prajapati, V. K. (2017). Exploring Leishmania secretory proteins to design B and T cell multi-epitope subunit vaccine using immunoinformatics approach. Scientific Reports, 7(1), 1–12. https://doi.org/10.1038/s41598-017-08842-w
   PubMed Web of Science ®Google Scholar
• Khoury, G. A., Smadbeck, J., Kieslich, C. A., Koskosidis, A. J., Guzman, Y. A., Tamamis, P., & Floudas, C. A. (2017). Princeton_TIGRESS 2.0: High refinement consistency and net gains through support vector machines and molecular dynamics in double-blind predictions during the CASP11 experiment. Proteins: Structure, Function, and Bioinformatics, 85(6), 1078–1098. [PubMed] https://doi.org/10.1002/prot.25274
   PubMed Web of Science ®Google Scholar
• Kohlgraf, K. G., Pingel, L. C., Dietrich, D. E., & Brogden, K. A. (2010). Defensins as anti-inflammatory compounds and mucosal adjuvants. Future Microbiology, 5(1), 99–113. https://doi.org/10.2217/fmb.09.104
   PubMed Web of Science ®Google Scholar
• Kozakov, D., Beglov, D., Bohnuud, T., Mottarella, S., 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
   PubMed Web of Science ®Google Scholar
• Larsen, M. V., Lundegaard, C., Lamberth, K., Buus, S., Lund, O., & Nielsen, M. (2007). Large-scale validation of methods for cytotoxic T-lymphocyte epitope prediction. BMC Bioinformatics, 8, 424. https://doi.org/10.1186/1471-2105-8-424
   PubMed Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• Lee, G. R., Heo, L., & Seok, C. (2016). Effective protein model structure refinement by loop modeling and overall relaxation. Proteins, 84(Suppl 1), 293–301. https://doi.org/10.1002/prot.24858
   PubMedGoogle Scholar
• Lee, S., & Nguyen, M. T. (2015). Recent advances of vaccine adjuvants for infectious diseases. Immune Network, 15(2), 51–57. https://doi.org/10.4110/in.2015.15.2.51
   PubMed Web of Science ®Google Scholar
• Lengauer, T., & Rarey, M. (1996). Computational methods for biomolecular docking. Current Opinion in Structural Biology, 6(3), 402–406. https://doi.org/10.1016/S0959-440X(96)80061-3
   PubMed Web of Science ®Google Scholar
• Lenz, O., ter Meulen, J., Klenk, H. D., Seidah, N. G., & Garten, W. (2001). The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proceedings of the National Academy of Sciences of the United States of America, 98(22), 12701–12705. https://doi.org/10.1073/pnas.221447598
   PubMed Web of Science ®Google Scholar
• Li, L., Vorobyov, I., & Allen, T. W. (2013). The different interactions of lysine and arginine side chains with lipid membranes. The Journal of Physical Chemistry. B, 117(40), 11906–11920. https://doi.org/10.1021/jp405418y
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins, 78(8), 1950–1958. https://doi.org/10.1002/prot.22711
   PubMed Web of Science ®Google Scholar
• Lorenz, R., Bernhart, S. H., Höner zu Siederdissen, C., Tafer, H., Flamm, C., Stadler, P. F., & Hofacker, I. L. (2011). ViennaRNA Package 2.0. Algorithms for Molecular Biology, 6, 26. https://doi.org/10.1186/1748-7188-6-26
   PubMed Web of Science ®Google Scholar
• Lukashevich, I. S., Paessler, S., & de la Torre, J. C. (2019). Lassa virus diversity and feasibilty for universal prophylactic vaccine. F1000Research, 8, 134. https://doi.org/10.12688/f1000research.16989.1
   Google Scholar
• Magnan, C. N., Arlo, R., & Pierre, B. (2009). SOLpro: Accurate sequence-based prediction of protein solubility. Bioinformatics, 25(17), 2200–2207. https://doi.org/10.1093/bioinformatics/btp386
   PubMed Web of Science ®Google Scholar
• Mahanty, S., Hutchinson, K., Agarwal, S., McRae, M., Rollin, P. E., & Pulendran, B. (2003). Cutting edge: Impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. Journal of Immunology, 170(6), 2797–2801. https://doi.org/10.4049/jimmunol.170.6.2797
   PubMed Web of Science ®Google Scholar
• Malfertheiner, P., Schultze, V., Rosenkranz, B., Kaufmann, S. H. E., Ulrichs, T., Novicki, D., Norelli, F., Contorni, M., Peppoloni, S., Berti, D., Tornese, D., Ganju, J., Palla, E., Rappuoli, R., Scharschmidt, B. F., & Del Giudice, G. (2008). Safety and immunogenicity of an intramuscular Helicobacter pylori vaccine in noninfected volunteers: A phase I study. Gastroenterology, 135(3), 787–795. https://doi.org/10.1053/j.gastro.2008.05.054
   PubMed Web of Science ®Google Scholar
• Maniatis, T., Fritsch, E. F., & Sambrook, J. (1982). Molecular cloning: A laboratory manual. Cold Spring Harbor University Press.
   Google Scholar
• Messaoudi, A., Belguith, H., & Hamida, J. B. (2013). Homology modeling and virtual screening approaches to identify potent inhibitors of VEB-1 β-lactamase. Theoretical Biology & Medical Modelling, 10(1), 20–22. https://doi.org/10.1186/1742-4682-10-22
   PubMedGoogle Scholar
• McCormick, J. B., & Fisher-Hoch, S. P. (2002). Lassa fever. Current Topics in Microbiology and Immunology, 262, 75–109. https://doi.org/10.1007/978-3-642-56029-3_4
   PubMed Web of Science ®Google Scholar
• Mehla, K., & Ramana, J. (2016). Identification of epitope-based peptide vaccine candidates against enterotoxigenic Escherichia coli: A comparative genomics and immunoinformatics approach. Molecular BioSystems, 12(3), 890–901. https://doi.org/10.1039/c5mb00745c
   PubMedGoogle Scholar
• 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, 49, 309–317. https://doi.org/10.1016/j.meegid.2017.02.007
   PubMed Web of Science ®Google Scholar
• Mirza, M. U., Rafique, S., Ali, A., Munir, M., Ikram, N., Manan, A., Salo-Ahen, O. M., & Idrees, M. (2016). Towards peptide vaccines against Zika virus: Immunoinformatics combined with molecular dynamics simulations to predict antigenic epitopes of Zika viral proteins. Scientific Reports, 6, 37313.
   PubMed Web of Science ®Google Scholar
• Möller, S., Croning, M., & Apweiler, R. (2001). Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics, 17(7), 646–653. DOI: 10/bioinformatics/17.7.646.
   PubMed Web of Science ®Google Scholar
• Morla, S., Makhija, A., & Kumar, S. (2016). Synonymous codon usage pattern in glycoprotein gene of rabies virus. Gene, 584(1), 1–6. https://doi.org/10.1016/j.gene.2016.02.047
   PubMed Web of Science ®Google Scholar
• Muhammad, S. A., Ashfaq, H., Zafar, S., Munir, F., Jamshed, M. B., Chen, J., & Zhang, Q. (2020). Polyvalent therapeutic vaccine for type 2 diabetes mellitus: Immunoinformatics approach to study co-stimulation of cytokines and GLUT1 receptors. BMC Molecular and Cell Biology, 21(1), 1–7. https://doi.org/10.1186/s12860-020-00279-w
   PubMed Web of Science ®Google Scholar
• Nagpal, G., Usmani, S. S., Dhanda, S. K., Kaur, H., Singh, S., Sharma, M., & Raghava, G. P. (2017). Computer-aided designing of immunosuppressive peptides based on IL-10 inducing potential. Scientific Reports, 7, 42851. https://doi.org/10.1038/srep42851
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Nigeria Centre for Disease Control (NCDC). (2020). Weekly epidemiological report. Retrieved 1/12/2020, from https://ncdc.gov.ng/reports/weekly
   Google Scholar
• Ogbu, O., Ajuluchukwu, E., & Uneke, C. J. (2007). Lassa fever in West African sub-region: An overview. Journal of Vector Borne Diseases, 44(1), 1–11.
   PubMedGoogle Scholar
• Olayemi, A., & Fichet-Calvet, E. (2020). Attributes affecting emergence of the Lassa virus in rodents across Western Africa. Viruses, 12(3), 312–543. https://doi.org/10.3390/v12030312
   PubMed Web of Science ®Google Scholar
• Pandey, R. K., Ojha, R., Aathmanathan, V. S., Krishnan, M., & Prajapati, V. K. (2018). Immunoinformatics approaches to design a novel multi-epitope subunit vaccine against HIV infection. Vaccine, 36(17), 2262–2272. https://doi.org/10.1016/j.vaccine.2018.03.042
   PubMed Web of Science ®Google Scholar
• Park, M. S., Kim, J. I., Lee, I., Park, S., Bae, J.-Y., & Park, M.-S. (2018). Towards the application of human defensins as antivirals. Biomolecules & Therapeutics, 26(3), 242–254. https://doi.org/10.4062/biomolther.2017.172
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1982). Strain fluctuations and elastic constants. Journal of Chemical Physics, 76(5), 2662–2666. https://doi.org/10.1063/1.443248
   Web of Science ®Google Scholar
• Patra, P., Mondal, N., Patra, B. C., & Bhattacharya, M. (2019). Epitope-based vaccine designing of Nocardia asteroides targeting the virulence factor Mce-family protein by immunoinformatics approach. International Journal of Peptide Research and Therapeutics, 26, 1165–1176. https://doi.org/10.1007/s10989-019-09921-4
   PubMed Web of Science ®Google Scholar
• Pavli, P., Hume, D. A., Van De Pol, E., & Doe, W. F. (1993). Dendritic cells, the major antigenpresenting cells of the human colonic lamina propria. Immunology, 78(1), 132.
   PubMed Web of Science ®Google Scholar
• Peters, B., Sidney, J., Bourne, P., Bui, H.-H., Buus, S., Doh, G., Fleri, W., Kronenberg, M., Kubo, R., Lund, O., Nemazee, D., Ponomarenko, J. V., Sathiamurthy, M., Schoenberger, S., Stewart, S., Surko, P., Way, S., Wilson, S., & Sette, A. (2005). The immune epitope database and analysis resource: From vision to blueprint. PLoS Biology, 3(3), e91. https://doi.org/10.1371/journal.pbio.0030091
   PubMed Web of Science ®Google Scholar
• Pickett, B. E., Sadat, E. L., Zhang, Y., Noronha, J. M., Squires, R. B., Hunt, V., Liu, M., Kumar, S., Zaremba, S., Gu, Z., Zhou, L., Larson, C. N., Dietrich, J., Klem, E. B., & Scheuermann, R. H. (2012). ViPR: An open bioinformatics database and analysis resource for virology research. Nucleic Acids Research, 40(Database issue), D593–D598. https://doi.org/10.1093/nar/gkr859
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Rahmani, A., Baee, M., Rostamtabar, M., Karkhah, A., Alizadeh, S., Tourani, M., & Reza, H. (2019). Development of a conserved chimeric vaccine based on helper T-cell and CTL epitopes for induction of strong immune response against Schistosoma mansoni using immunoinformatics approaches. International Journal of Biological Macromolecules, 141, 125–136. https://doi.org/10.1016/j.ijbiomac.2019.08.259
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Rapin, N., Lund, O., & Castiglione, F. (2011). Immune system simulation online. Bioinformatics, 27(14), 2013–2014. https://doi.org/10.1093/bioinformatics/btr335
   PubMed Web of Science ®Google Scholar
• Reji, M. I. (2013). Computation of molecular weight of proteins. Proceedings of UGC Sponsored Third National Conference on Modern Trends in Electronic Communication & Signal Processing (NCMES-2013), Department of Electronics, BPC College.
   Google Scholar
• Rosano, G. L., & Ceccarelli, E. A. (2014). Recombinant protein expression in Escherichia coli: Advances and challenges. Frontiers in Microbiology, 5, 1–17. https://doi.org/10.3389/fmicb.2014.00172
   PubMed Web of Science ®Google Scholar
• Rossi, G., Ruggiero, P., Peppoloni, S., Pancotto, L., Fortuna, D., Lauretti, L., Volpini, G., Mancianti, S., Corazza, M., Taccini, E., Di Pisa, F., Rappuoli, R., & Del Giudice, G. (2004). Therapeutic vaccination against Helicobacter pylori in the Beagle Dog Experimental Model: Safety, immunogenicity, and efficacy. Infection and Immunity, 72(6), 3252–3259. https://doi.org/10.1128/IAI.72.6.3252-3259.2004
   PubMed Web of Science ®Google Scholar
• Safronetz, D., Lopez, J. E., Sogoba, N., Traore', S. F., Raffel, S. J., Fischer, E. R., Ebihara, H., Branco, L., Garry, R. F., Schwan, T. G., & Feldmann, H. (2010). Detection of Lassa virus, Mali. Emerging Infectious Diseases, 16(7), 1123–1126. https://doi.org/10.3201/eid1607.100146
   PubMed Web of Science ®Google Scholar
• Sarkar, B., Ullah, M. A., Araf, Y., & Rahman, M. S. (2020a). Engineering a novel subunit vaccine against SARS-CoV-2 by exploring immunoinformatics approach. Informatics in Medicine Unlocked, 21, 100478. https://doi.org/10.1016/j.imu.2020.100478
   PubMedGoogle Scholar
• Sarkar, B., Ullah, M. A., & Araf, Y. (2020b). A systematic and reverse vaccinology approach to design novel subunit vaccines against Dengue virus Type-1 and human papillomavirus-16. Informatics in Medicine Unlocked, 19, 100343. https://doi.org/10.1016/j.imu.2020
   Google Scholar
• Schneidman-Duhovny, D., Inbar, Y., Nussinov, R., & Wolfson, H. J. (2005). PatchDock and SymmDock: Servers for rigid and symmetric docking. Nucleic Acids Research, 33(Web Server issue), W363–W367. https://doi.org/10.1093/nar/gki481
   PubMed Web of Science ®Google Scholar
• Shahid, F., Ashfaq, U. A., Javaid, A., & Khalid, H. (2020). Immunoinformatics guided rational design of a next generation multi epitope based peptide (MEBP) vaccine by exploring Zika virus proteome. Infection, Genetics and Evolution, 80, 104199. https://doi.org/10.1016/j.meegid.2020.104199
   PubMed Web of Science ®Google Scholar
• Shamriz, S., Ofoghi, H., & Moazami, N. (2016). Effect of linker length and residues on the structure and stability of a fusion protein with malaria vaccine application. Computers in Biology and Medicine, 76, 24–29. https://doi.org/10.1016/j.compbiomed.2016.06.015
   PubMed Web of Science ®Google Scholar
• Sharp, P. M., & Li, W. H. (1987). The Codon Adaptation Index – A measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 15(3), 1281–1295. https://doi.org/10.1093/nar/15.3.1281
   PubMed Web of Science ®Google Scholar
• Shey, R. A., Ghogomu, S. M., Esoh, K. K., Nebangwa, N. D., Shintouo, C. M., Nongley, N. F., Asa, B. F., Ngale, F. N., Vanhamme, L., & Souopgui, J. (2019). In-silico design of a multi-epitope vaccine candidate against onchocerciasis and related filarial diseases. Scientific Reports, 9(1), 1–18. https://doi.org/10.1038/s41598-019-40833-x
   PubMed Web of Science ®Google Scholar
• Siddle, K. J., Eromon, P., Barnes, K. G., Mehta, S., Oguzie, J. U., Odia, I., Schaffner, S. F., Winnicki, S. M., Shah, R. R., Qu, J., Wohl, S., Brehio, P., Iruolagbe, C., Aiyepada, J., Uyigue, E., Akhilomen, P., Okonofua, G., Ye, S., Kayode, T., … Happi, C. T. (2018). Genomic analysis of Lassa virus during an increase in cases in Nigeria in 2018. The New England Journal of Medicine, 379(18), 1745–1753. https://doi.org/10.1056/NEJMoa1804498
   PubMed Web of Science ®Google Scholar
• Tanchot, C., & Rocha, B. (2003). CD8 and B cell memory: Same strategy, same signals. Nature Immunology, 4(5), 431–432. https://doi.org/10.1038/ni0503-431
   PubMed Web of Science ®Google Scholar
• Tosta, S. F., Passos, M. S., Kato, R., Salgado, Á., Xavier, J., Jaiswal, A. K., Soares, S. C., Azevedo, V., Giovanetti, M., Tiwari, S., & Alcantara, L. C. (2021). Multi-epitope based vaccine against yellow fever virus applying immunoinformatics approaches. Journal of Biomolecular Structure and Dynamics, 39(1), 219–235. https://doi.org/10.1080/07391102.2019.1707120
   PubMed Web of Science ®Google Scholar
• Vajda, S., Yueh, C., Beglov, D., Bohnuud, T., Mottarella, S. E., Xia, B., Hall, D. R., & Kozakov, D. (2017). New additions to the ClusPro server motivated by CAPRI. Proteins, 85(3), 435–444. https://doi.org/10.1002/prot.25219
   PubMed Web of Science ®Google Scholar
• Vita, R., Overton, J. A., Greenbaum, J. A., Ponomarenko, J., Clark, J. D., Cantrell, J. R., Wheeler, D. K., Gabbard, J. L., Hix, D., Sette, A., & Peters, B. (2015). The immune epitope database (IEDB) 3.0. Nucleic Acids Research, 43(Database issue), D405–D12. https://doi.org/10.1093/nar/gku938
   PubMed Web of Science ®Google Scholar
• Vogel, D., Rosenthal, M., Gogrefe, N., Reindl, S., & Günther, S. (2019). Biochemical characterization of the Lassa virus L protein. The Journal of Biological Chemistry, 294(20), 8088–8100. . https://doi.org/10.1074/jbc.RA118.006973
   PubMed Web of Science ®Google Scholar
• Wang, P., Sidney, J., Kim, Y., Sette, A., Lund, O., Nielsen, M., & Peters, B. (2010). Peptide binding predictions for HLA DR, DP and DQ molecules. BMC Bioinformatics, 11(1), 568. https://doi.org/10.1186/1471-2105-11-568
   PubMed Web of Science ®Google Scholar
• Watanabe, Y., Raghwani, J., Allen, J. D., Seabright, G. E., Li, S., Moser, F., Huiskonen, J. T., Strecker, T., Bowden, T. A., & Crispin, M. (2018). Structure of the Lassa virus glycan shield provides a model for immunological resistance. Proceedings of the National Academy of Sciences of the United States of America, 115(28), 7320–7325. https://doi.org/10.1073/pnas.1803990115
   PubMed Web of Science ®Google Scholar
• Weinberg, A., Jin, G., Sieg, S., & McCormick, T. S. (2012). The yin and yang of human Beta-defensins in health and disease. Frontiers in Immunology, 3, 294. https://doi.org/10.3389/fimmu.2012.00294
   PubMed Web of Science ®Google Scholar
• World Health Organization (WHO). (2020). Lassa fever – Nigeria. Retrieved 1/12/2020, from https://www.who.int/csr/don/20-february-2020-lassa-fever-nigeria/en/
   Google Scholar
• Xing, J., Ly, H., & Liang, Y. (2015). The Z proteins of pathogenic but not nonpathogenic arenaviruses inhibit RIG-I-like receptor-dependent interferon production. Journal of Virology, 89(5), 2944–2955. https://doi.org/10.1128/JVI.03349-14
   PubMed Web of Science ®Google Scholar
• Yin, D., Li, L., Song, X., Li, H., Wang, J., Ju, W., Qu, X., Song, D., Liu, Y., Meng, X., Cao, H., Song, W., Meng, R., Liu, J., Li, J., & Xu, K. (2016). A novel multi-epitope recombined protein for diagnosis of human brucellosis. BMC Infectious Diseases, 16, 219.
   PubMed Web of Science ®Google Scholar
• Yun, N. E., & Walker, D. H. (2012). Pathogenesis of Lassa fever. Viruses, 4(10), 2031–2048. https://doi.org/10.3390/v4102031
   PubMed Web of Science ®Google Scholar
• Zinzula, L., & Tramontano, E. (2013). Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: Hide, mask, hit. Antiviral Research, 100(3), 615–635. https://doi.org/10.1016/j.antiviral.2013.10.002
   PubMed Web of Science ®Google Scholar