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Research Articles

Immunoinformatic-guided novel mRNA vaccine designing to elicit immunogenic responses against the endemic Monkeypox virus

, , , , , , , , & show all
Pages 6292-6306 | Received 17 Feb 2023, Accepted 01 Jul 2023, Published online: 09 Jul 2023

References

  • No author (2011). Monkeypox. Wkly Epidemiol Record, 86, 448–451.
  • No author (2022). Monkeypox virus preparation in Pakistan-Next viral zoonotic disease outbreak after COVID-19? Biomedical Letters, 8, 196–201.
  • 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
  • Ahammad, I., & Lira, S. S. (2020). Designing a novel mRNA vaccine against SARS-CoV-2: An immunoinformatics approach. International Journal of Biological Macromolecules, 162, 820–837. https://doi.org/10.1016/j.ijbiomac.2020.06.213
  • Aiman, S., Alhamhoom, Y., Ali, F., Rahman, N., Rastrelli, L., Khan, A., Farooq, Q. U. A., Ahmed, A., Khan, A., & Li, C. (2022a). Multi-epitope chimeric vaccine design against emerging Monkeypox virus via reverse vaccinology techniques- a bioinformatics and immunoinformatics approach. Frontiers in Immunology, 13, 985450. https://doi.org/10.3389/fimmu.2022.985450
  • Aiman, S., Ali, F., Zia, A., Aslam, M., Han, Z., Shams, S., Khan, A., & Li, C. (2022b). Core genome mediated potential vaccine targets prioritization against Clostridium difficile via reverse vaccinology-an immuno-informatics approach. Journal of Biological Research 29, 6.
  • Al Tbeishat, H. (2022). Novel In Silico mRNA vaccine design exploiting proteins of M. tuberculosis that modulates host immune responses by inducing epigenetic modifications. Scientific Reports, 12(1), 4645. https://doi.org/10.1038/s41598-022-08506-4
  • Alakunle, E., Moens, U., Nchinda, G., & Okeke, M. I. (2020). Monkeypox Virus in Nigeria: Infection Biology, Epidemiology, and Evolution. Viruses, 12(11), 1257. https://doi.org/10.3390/v12111257
  • Alberer, M., Gnad-Vogt, U., Hong, H. S., Mehr, K. T., Backert, L., Finak, G., Gottardo, R., Bica, M. A., Garofano, A., Koch, S. D., Fotin-Mleczek, M., Hoerr, I., Clemens, R., & VON Sonnenburg, F. (2017). Safety and immunogenicity of a mRNA rabies vaccine in healthy adults: An open-label, non-randomised, prospective, first-in-human phase 1 clinical trial. Lancet (London, England), 390(10101), 1511–1520. https://doi.org/10.1016/S0140-6736(17)31665-3
  • Aslam, M., Shehroz, M., Shah, M., Khan, M. A., Afridi, S. G., Khan, A, 2020. Potential druggable proteins and chimeric vaccine construct prioritization against Brucella melitensis from species core genome data. Genomics, 112, 1734–1745. https://doi.org/10.1016/j.ygeno.2019.10.009
  • Babkin, I. V., Babkina, I. N., & Tikunova, N. V. (2022). An update of orthopoxvirus molecular evolution. Viruses, 14(2), 388. https://doi.org/10.3390/v14020388
  • Bahl, K., Senn, J. J., Yuzhakov, O., Bulychev, A., Brito, L. A., Hassett, K. J., Laska, M. E., Smith, M., Almarsson, Ö., Thompson, J., Ribeiro, A. M., Watson, M., Zaks, T., & Ciaramella, G. (2017). Preclinical and clinical demonstration of immunogenicity by mRNA vaccines against H10N8 and H7N9 influenza viruses. Molecular Therapy : The Journal of the American Society of Gene Therapy, 25(6), 1316–1327. https://doi.org/10.1016/j.ymthe.2017.03.035
  • Baptista-Hon, D. T., Fesalbon, G. J. W., & Monteiro, O. (2022). Changing clinical features of the 2022 monkeypox global health emergency. MedComm – Future Medicine, 1(2), e24. https://doi.org/10.1002/mef2.24
  • Baum, L. L., Mathieson, B. J., & Connick, E. (2016). Immunity to HIV. In Ratcliffe, M. J. H. (Ed.). Encyclopedia of Immunobiology. Academic Press.
  • Bibi, S., Ullah, I., Zhu, B., Adnan, M., Liaqat, R., Kong, W.-B., & Niu, S. (2021). In silico analysis of epitope-based vaccine candidate against tuberculosis using reverse vaccinology. Scientific Reports, 11(1), 1249. https://doi.org/10.1038/s41598-020-80899-6
  • 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
  • Bui, H.-H., Sidney, J., Dinh, K., Southwood, S., Newman, M. J., & Sette, A. (2006). Predicting population coverage of T-cell epitope-based diagnostics and vaccines. BMC Bioinformatics, 7, 153. https://doi.org/10.1186/1471-2105-7-153
  • Bui, H.-H., Sidney, J., Li, W., Fusseder, N., & Sette, A. (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
  • 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
  • Chaplin, D. D. (2010). Overview of the immune response. The Journal of Allergy and Clinical Immunology, 125(2 Suppl 2), S3–S23. https://doi.org/10.1016/j.jaci.2009.12.980
  • Chen, H., Wu, B., Zhang, T., Jia, J., Lu, J., Chen, Z., Ni, Z., & Tan, T. (2017a). Effect of linker length and flexibility on the clostridium thermocellum esterase displayed on bacillus subtilis spores. Applied Biochemistry and Biotechnology, 182(1), 168–180. https://doi.org/10.1007/s12010-016-2318-y
  • Chen, N., Xia, P., Li, S., Zhang, T., Wang, T. T., & Zhu, J. (2017b). RNA sensors of the innate immune system and their detection of pathogens. IUBMB Life, 69(5), 297–304. https://doi.org/10.1002/iub.1625
  • Dimitrov, I., Flower, D. R., & Doytchinova, I. (2013). AllerTOP–a server for in silico prediction of allergens. BMC Bioinformatics, 14 Suppl 6(Suppl 6), S4. https://doi.org/10.1186/1471-2105-14-S6-S4
  • Dörner, T., & Radbruch, A. (2007). Antibodies and B Cell Memory in Viral Immunity. Immunity, 27(3), 384–392. https://doi.org/10.1016/j.immuni.2007.09.002
  • 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
  • Fadaka, A. O., Sibuyi, N. R. S., Martin, D. R., Goboza, M., Klein, A., Madiehe, A. M., & Meyer, M. (2021). Immunoinformatics design of a novel epitope-based vaccine candidate against dengue virus. Scientific Reports, 11(1), 19707. https://doi.org/10.1038/s41598-021-99227-7
  • Gandhi, R. T., Kwon, D. S., Macklin, E. A., Shopis, J. R., Mclean, A. P., Mcbrine, N., Flynn, T., Peter, L., Sbrolla, A., Kaufmann, D. E., Porichis, F., Walker, B. D., Bhardwaj, N., Barouch, D. H., & Kavanagh, D. G. (2016). Immunization of HIV-1-Infected persons with autologous dendritic cells transfected with mRNA Encoding HIV-1 Gag and Nef: results of a randomized, placebo-controlled clinical trial. Journal of Acquired Immune Deficiency Syndromes (1999), 71(3), 246–253. https://doi.org/10.1097/QAI.0000000000000852
  • Garg, A., & Gupta, D. (2008). VirulentPred: A SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinformatics, 9, 62. https://doi.org/10.1186/1471-2105-9-62
  • Geourjon, C., & Deléage, G. (1995). SOPMA: Significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Computer Applications in the Biosciences : CABIOS, 11(6), 681–684. https://doi.org/10.1093/bioinformatics/11.6.681
  • Gergen, J., & Petsch, B. (2021). mRNA-based vaccines and mode of action. Current Topics in Microbiology and Immunology, 440, 1–30.
  • Grant, R., Nguyen, L. L., & Breban, R. (2020). Modelling human-to-human transmission of monkeypox. Bulletin of the World Health Organization, 98(9), 638–640. https://doi.org/10.2471/BLT.19.242347
  • Gruber, A. R., Lorenz, R., Bernhart, S. H., Neuböck, R., & Hofacker, I. L. (2008). The Vienna RNA websuite. Nucleic Acids Research, 36(Web Server issue), W70–4. https://doi.org/10.1093/nar/gkn188
  • Gupta, S., Kapoor, P., Chaudhary, K., Gautam, A., Kumar, R., Open Source Drug Discovery, C., & Raghava, G. P. S, 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
  • Hammarlund, E., Lewis, M. W., Carter, S. V., Amanna, I., Hansen, S. G., Strelow, L. I., Wong, S. W., Yoshihara, P., Hanifin, J. M., & Slifka, M. K. (2005). Multiple diagnostic techniques identify previously vaccinated individuals with protective immunity against monkeypox. Nature Medicine, 11(9), 1005–1011. https://doi.org/10.1038/nm1273
  • Heo, L., Park, H., & Seok, C. (2013). GalaxyRefine: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41(Web Server issue), W384–8. https://doi.org/10.1093/nar/gkt458
  • Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review. A, General Physics, 31(3), 1695–1697. https://doi.org/10.1103/physreva.31.1695
  • Huang, Y., Niu, B., Gao, Y., Fu, L., & Li, W. (2010). CD-HIT Suite: A web server for clustering and comparing biological sequences. Bioinformatics (Oxford, England), 26(5), 680–682. https://doi.org/10.1093/bioinformatics/btq003
  • Humphreys, D. D., Friesner, R. A., & Berne, B. J. (1994). A multiple-time-step molecular dynamics algorithm for macromolecules. The Journal of Physical Chemistry, 98(27), 6885–6892. https://doi.org/10.1021/j100078a035
  • Ismail, S., Abbasi, S. W., Yousaf, M., Ahmad, S., Muhammad, K., & Waheed, Y. (2022). Design of a multi-epitopes vaccine against hantaviruses: an immunoinformatics and molecular modelling approach. Vaccines, 10(3), 378. https://doi.org/10.3390/vaccines10030378
  • Jaan, S., Zaman, A., Ahmed, S., Shah, M., & Ojha, S. C. (2022). mRNA vaccine designing using chikungunya virus e glycoprotein through immunoinformatics-guided approaches. Vaccines, 10(9), 1476. https://doi.org/10.3390/vaccines10091476
  • Jahangirian, E., Jamal, G. A., Nouroozi, M., & Mohammadpour, A. (2021). A reverse vaccinology and immunoinformatics approach for designing a multiepitope vaccine against SARS-CoV-2. Immunogenetics, 73(6), 459–477. https://doi.org/10.1007/s00251-021-01228-3
  • Jalal, K., Khan, K., Basharat, Z., Abbas, M. N., Uddin, R., Ali, F., Khan, S. A., & Hassan, S. S. U. (2022). Reverse vaccinology approach for multi-epitope centered vaccine design against delta variant of the SARS-CoV-2. Environmental Science and Pollution Research International, 29(40), 60035–60053. https://doi.org/10.1007/s11356-022-19979-1
  • Jorgensen, W., Chandrasekhar, J., Madura, J., Impey, R., & Klein, M. (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics. 79(2), 926–935. https://doi.org/10.1063/1.445869
  • Kakakhel, S., Ahmad, A., Mahdi, W. A., Alshehri, S., Aiman, S., Begum, S., Shams, S., Kamal, M., Imran, M., Shakeel, F., & Khan, A. (2023). Annotation of potential vaccine targets and designing of mRNA-based multi-epitope vaccine against lumpy skin disease virus via reverse vaccinology and agent-based modeling. Bioengineering, 10(4), 430. [Online], https://doi.org/10.3390/bioengineering10040430
  • Kalia, V., Sarkar, S., Gourley, T. S., Rouse, B. T., & Ahmed, R. (2006). Differentiation of memory B and T cells. Current Opinion in Immunology, 18(3), 255–264. https://doi.org/10.1016/j.coi.2006.03.020
  • Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845–858. https://doi.org/10.1038/nprot.2015.053
  • Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
  • 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
  • Kräutler, V., van Gunsteren, W. F., & Hünenberger, P. H. (2001). A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. Journal of Computational Chemistry, 22(5), 501–508. https://doi.org/10.1002/1096-987X(20010415)22:5<501::AID-JCC1021>3.0.CO;2-V
  • Kreiter, S., Selmi, A., Diken, M., Sebastian, M., Osterloh, P., Schild, H., Huber, C., Türeci, O., & Sahin, U. (2008). Increased antigen presentation efficiency by coupling antigens to MHC class I trafficking signals. Journal of Immunology, 180(1), 309–318. https://doi.org/10.4049/jimmunol.180.1.309
  • Kumari, R., Kumar, R., & Lynn, A, Open Source Drug Discovery Consortium. (2014). g_mmpbsa–a GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
  • Ladnyj, I. D., Ziegler, P., & Kima, E. (1972). A human infection caused by monkeypox virus in Basankusu Territory, Democratic Republic of the Congo. Bulletin of the World Health Organization, 46(5), 593–597.
  • Le, T. K., Paris, C., Khan, K. S., Robson, F., Ng, W.-L., & Rocchi, P. (2021). Nucleic acid-based technologies targeting coronaviruses. Trends in Biochemical Sciences, 46(5), 351–365. https://doi.org/10.1016/j.tibs.2020.11.010
  • 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
  • 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 : AMB, 6, 26. https://doi.org/10.1186/1748-7188-6-26
  • Lovell, S. C., Davis, I. W., Arendall, W. B., de Bakker, P. I. W., Word, J. M., Prisant, M. G., Richardson, J. S., & Richardson, D. C. (2003). Structure validation by Cα geometry: ϕ,ψ and Cβ deviation. Proteins: Structure, Function, and Bioinformatics, 50(3), 437–450. https://doi.org/10.1002/prot.10286
  • Lu, C., Wu, C., Ghoreishi, D., Chen, W., Wang, L., Damm, W., Ross, G. A., Dahlgren, M. K., Russell, E., VON Bargen, C. D., Abel, R., Friesner, R. A., & Harder, E. D. (2021). OPLS4: improving force field accuracy on challenging regimes of chemical space. Journal of Chemical Theory and Computation, 17(7), 4291–4300. https://doi.org/10.1021/acs.jctc.1c00302
  • 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
  • Mccollum, A. M., & Damon, I. K. (2014). Human monkeypox. Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 58(2), 260–267. https://doi.org/10.1093/cid/cit703
  • Mishra, S., Rout, M., Panda, S., Singh, S. K., Sinha, R., Dehury, B., & Pati, S. (2023). An immunoinformatic approach towards development of a potent and effective multi-epitope vaccine against monkeypox virus (MPXV). Journal of Biomolecular Structure and Dynamics, 41, 1–14. https://doi.org/10.1080/07391102.2022.2163426
  • Mustafa, M. I., Shantier, S. W., Abdelmageed, M. I., & Makhawi, A. M. J. I. I. M. U. (2021). Epitope-based peptide vaccine against Bombali Ebolavirus viral protein 40: An immunoinformatics combined with molecular docking studies. Informatics in Medicine Unlocked, 25, 100694. https://doi.org/10.1016/j.imu.2021.100694
  • Nain, Z., Abdulla, F., Rahman, M. M., Karim, M. M., Khan, M. S. A., Sayed, S. B., Mahmud, S., Rahman, S. M. R., Sheam, M. M., Haque, Z., & Adhikari, U. K. (2020). Proteome-wide screening for designing a multi-epitope vaccine against emerging pathogen Elizabethkingia anophelis using immunoinformatic approaches. Journal of Biomolecular Structure & Dynamics, 38(16), 4850–4867. https://doi.org/10.1080/07391102.2019.1692072
  • Nezafat, N., Karimi, Z., Eslami, M., Mohkam, M., Zandian, S., & Ghasemi, Y. (2016). Designing an efficient multi-epitope peptide vaccine against Vibrio cholerae via combined immunoinformatics and protein interaction based approaches. Computational Biology and Chemistry, 62, 82–95. https://doi.org/10.1016/j.compbiolchem.2016.04.006
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera—A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • 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), D593–8. https://doi.org/10.1093/nar/gkr859
  • 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
  • Richner, J. M., Himansu, S., Dowd, K. A., Butler, S. L., Salazar, V., Fox, J. M., Julander, J. G., Tang, W. W., Shresta, S., Pierson, T. C., Ciaramella, G., & Diamond, M. S. (2017). Modified mRNA vaccines protect against zika virus infection. Cell, 168(6), 1114–1125.e10. https://doi.org/10.1016/j.cell.2017.02.017
  • Rosendahl Huber, S., VAN Beek, J., DE Jonge, J., Luytjes, W., & VAN Baarle, D. (2014). T cell responses to viral infections - opportunities for Peptide vaccination. Frontiers in Immunology, 5, 171. https://doi.org/10.3389/fimmu.2014.00171
  • Rotz, L. D., Dotson, D. A., Damon, I. K., & Becher, J. A, Advisory Committee on Immunization Practices. (2001). Vaccinia (smallpox) vaccine: Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2001. MMWR. Recommendations and Reports : Morbidity and Mortality Weekly Report. Recommendations and Reports, 50(RR-10), 1–25. quiz CE1-7.
  • Saha, S., & Raghava, G. P. (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
  • Sette, A., & Rappuoli, R. (2010). Reverse Vaccinology: Developing Vaccines in the Era of Genomics. Immunity, 33(4), 530–541. https://doi.org/10.1016/j.immuni.2010.09.017
  • Shaik, M. S., Liem, S. Y., & Popelier, P. L. (2010). Properties of liquid water from a systematic refinement of a high-rank multipolar electrostatic potential. The Journal of Chemical Physics, 132(17), 174504. https://doi.org/10.1063/1.3409563
  • Shantier, S. W., Mustafa, M. I., Abdelmoneim, A. H., Fadl, H. A., Elbager, S. G., & Makhawi, A. M. (2022). Novel multi epitope-based vaccine against monkeypox virus: Vaccinomic approach. Scientific Reports, 12(1), 15983. https://doi.org/10.1038/s41598-022-20397-z
  • Shaw, D. E. (2005). A fast, scalable method for the parallel evaluation of distance-limited pairwise particle interactions. Journal of Computational Chemistry, 26(13), 1318–1328. https://doi.org/10.1002/jcc.20267
  • Sklenovská, N., & VAN Ranst, M. (2018). Emergence of monkeypox as the most important orthopoxvirus infection in humans. Frontiers in Public Health, 6, 241. https://doi.org/10.3389/fpubh.2018.00241
  • Tandrup Schmidt, S., Foged, C., Korsholm, K. S., Rades, T., & Christensen, D. (2016). Liposome-based adjuvants for subunit vaccines: formulation strategies for subunit antigens and immunostimulators. Pharmaceutics, 8(1), 7. https://doi.org/10.3390/pharmaceutics8010007
  • Tsui, N. B. Y., Ng, E. K. O., & Lo, Y. M. D. (2002). Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clinical Chemistry, 48(10), 1647–1653.
  • Waltz, K. N. (1993). The new world order. Millennium: Journal of International Studies, 22(2), 187–195. https://doi.org/10.1177/03058298930220020801
  • Waqas, M., Aziz, S., Liò, P., Khan, Y., Ali, A., Iqbal, A., Khan, F., & Almajhdi, F. N. (2023). Immunoinformatics design of multivalent epitope vaccine against monkeypox virus and its variants using membrane-bound, enveloped. And Extracellular Proteins as Targets, 14, 1091941.
  • Warny, M., Pepin, J., Fang, A., Killgore, G., Thompson, A., Brazier, J., Frost, E., & Mcdonald, L. C. (2005). Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet, 366(9491), 1079–1084. https://doi.org/10.1016/S0140-6736(05)67420-X
  • 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), W407–10. https://doi.org/10.1093/nar/gkm290
  • Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., & Hochstrasser, D. F. (1999). Protein identification and analysis tools in the ExPASy server. Methods in Molecular Biology (Clifton, N.J.), 112, 531–552. https://doi.org/10.1385/1-59259-584-7:531
  • Wolff, J. A., Malone, R. W., Williams, P., Chong, W., Acsadi, G., Jani, A., & Felgner, P. L. (1990). Direct gene transfer into mouse muscle in vivo. Science (New York, N.Y.), 247(4949 Pt 1), 1465–1468. https://doi.org/10.1126/science.1690918
  • Wu, F., Bhansali, S. G., Law, W. C., Bergey, E. J., Prasad, P. N., & Morris, M. E. (2012). Fluorescence imaging of the lymph node uptake of proteins in mice after subcutaneous injection: Molecular weight dependence. Pharmaceutical Research, 29(7), 1843–1853. https://doi.org/10.1007/s11095-012-0708-6
  • Xu, S., Yang, K., Li, R., & Zhang, L. (2020). mRNA Vaccine Era-Mechanisms, Drug Platform and Clinical Prospection. International Journal of Molecular Sciences, 21, 6582.
  • 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
  • Yousaf, M., Ismail, S., Ullah, A., & Bibi, S. (2022). Immuno-informatics profiling of monkeypox virus cell surface binding protein for designing a next generation multi-valent peptide-based vaccine. Frontiers in Immunology, 13, 1035924. https://doi.org/10.3389/fimmu.2022.1035924
  • Zhang, L. (2018). Multi-epitope vaccines: A promising strategy against tumors and viral infections. Cellular & Molecular Immunology, 15(2), 182–184. https://doi.org/10.1038/cmi.2017.92

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