262
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Computational vaccinology guided design of multi-epitope subunit vaccine against a neglected arbovirus of the Americas

, , , , &
Pages 3321-3338 | Received 24 Jan 2022, Accepted 22 Feb 2022, Published online: 14 Mar 2022

References

  • Abad-Franch, F., Grimmer, G. H., de Paula, V. S., Figueiredo, L. T. M., Braga, W. S. M., & Luz, S. L. B. (2012). Mayaro virus infection in Amazonia: A multimodel inference approach to risk factor assessment. PLoS Neglected Tropical Diseases, 6(10), e1846. https://doi.org/10.1371/journal.pntd.0001846
  • Abdulla, F., Adhikari, U. K., & Uddin, M. K. (2019). Exploring t & b-cell epitopes and designing multi-epitope subunit vaccine targeting integration step of hiv-1 lifecycle using immunoinformatics approach. Microbial Pathogenesis, 137, 103791. https://doi.org/10.1016/j.micpath.2019.103791
  • Ahola, T., & Kääriäinen, L. (1995). Reaction in alphavirus mRNA capping: Formation of a covalent complex of nonstructural protein nsp1 with 7-methyl-gmp. Proceedings of the National Academy of Sciences of the United States of America, 92(2), 507–511. https://doi.org/10.1073/pnas.92.2.507
  • Anderson, C., Downs, W. G., & Wattlby, G. (1957). Mayaro virus: A new human disease agent. ii. Isolation from blood of patients in Trinidad, BWI. American Journal of Tropical Medicine and Hygiene, 6(6), 1012-1016. https://doi.org/10.4269/ajtmh.1957.6.1012
  • Auguste, A. J., Liria, J., Forrester, N. L., Giambalvo, D., Moncada, M., Long, K. C., Morón, D., de Manzione, N., Tesh, R. B., Halsey, E. S., Kochel, T. J., Hernandez, R., Navarro, J.-C., & Weaver, S. C. (2015). Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases, 21(10), 1742–1750. https://doi.org/10.3201/eid2110.141660
  • Barone, V., Biczysko, M., & Brancato, G. (2010). Extending the range of computational spectroscopy by qm/mm approaches: Time-dependent and time-independent routes. Advances in Quantum Chemistry, 59, 17–58.
  • Bhattacharya, M., Sharma, A. R., Patra, P., Ghosh, P., Sharma, G., Patra, B. C., Lee, S.-S., & Chakraborty, C. (2020). Development of epitope-based peptide vaccine against novel coronavirus 2019 (sars-cov-2): Immunoinformatics approach. Journal of Medical Virology, 92(6), 618–631. https://doi.org/10.1002/jmv.25736
  • Brinton, M. A. (2002). The molecular biology of west Nile virus: A new invader of the western hemisphere. Annual Review of Microbiology, 56(1), 371–402. https://doi.org/10.1146/annurev.micro.56.012302.160654
  • Brooijmans, N., & Kuntz, I. D. (2003). Molecular recognition and docking algorithms. Annual Review of Biophysics and Biomolecular Structure, 32(1), 335–373. https://doi.org/10.1146/annurev.biophys.32.110601.142532
  • Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). Charmm: The biomolecular simulation program. Journal of Computational Chemistry, 30(10), 1545–1614. https://doi.org/10.1002/jcc.21287
  • 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(1), 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(1), 361. https://doi.org/10.1186/1471-2105-8-361
  • Burger, S. K., Thompson, D. C., & Ayers, P. W. (2011). Quantum mechanics/molecular mechanics strategies for docking pose refinement: Distinguishing between binders and decoys in cytochrome c peroxidase. Journal of Chemical Information and Modeling, 51(1), 93–101. https://doi.org/10.1021/ci100329z
  • Chabot, I., Goetghebeur, M. M., & Grégoire, J. P. (2004). The societal value of universal childhood vaccination. Vaccine, 22(15–16), 1992–2005. https://doi.org/10.1016/j.vaccine.2003.10.027
  • Chakraborty, S., Barman, A., & Deb, B. (2020). Japanese encephalitis virus: A multi-epitope loaded peptide vaccine formulation using reverse vaccinology approach. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 78, 104106. https://doi.org/10.1016/j.meegid.2019.104106
  • Chen, J., Sawyer, N., & Regan, L. (2013). Protein-protein interactions: general trends in the relationship between binding affinity and interfacial buried surface area. Protein Science: A Publication of the Protein Society, 22(4), 510–515. https://doi.org/10.1002/pro.2230
  • Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., & Richardson, D. C. (2010). Molprobity: All-atom structure validation for macromolecular crystallography. Acta Crystallographica. Section D, Biological Crystallography, 66(Pt 1), 12–21. https://doi.org/10.1107/S0907444909042073
  • Cho, A. E., Chung, J. Y., Kim, M., & Park, K. (2009). Quantum mechanical scoring for protein docking. The Journal of Chemical Physics, 131(13), 134108. https://doi.org/10.1063/1.3239504
  • Cho, A. E., Guallar, V., Berne, B. J., & Friesner, R. (2005). Importance of accurate charges in molecular docking: Quantum mechanical/molecular mechanical (qm/mm) approach. Journal of Computational Chemistry, 26(9), 915–931. https://doi.org/10.1002/jcc.20222
  • Chung, L. W., Sameera, W. M. C., Ramozzi, R., Page, A. J., Hatanaka, M., Petrova, G. P., Harris, T. V., Li, X., Ke, Z., Liu, F., Li, H.-B., Ding, L., & Morokuma, K. (2015). The oniom method and its applications. Chemical Reviews, 115(12), 5678–5796. https://doi.org/10.1021/cr5004419
  • Coimbra, T. L. M., Santos, C. L. S., Suzuki, A., Petrella, S. M. C., Bisordi, I., Nagamori, A. H., Marti, A. T., Santos, R. N., Fialho, D. M., Lavigne, S., Buzzar, M. R., & Rocco, I. M. (2007). Mayaro virus: Imported cases of human infection in são paulo state, brazil. Revista Do Instituto de Medicina Tropical de Sao Paulo, 49(4), 221–224. https://doi.org/10.1590/s0036-46652007000400005
  • Dar, H., Zaheer, T., Rehman, M. T., Ali, A., Javed, A., Khan, G. A., Babar, M. M., & Waheed, Y. (2016). Prediction of promiscuous t-cell epitopes in the zika virus polyprotein: An in silico approach. Asian Pacific Journal of Tropical Medicine, 9(9), 844–850. https://doi.org/10.1016/j.apjtm.2016.07.004
  • Dey, S., Nandy, A., Basak, S. C., Nandy, P., & Das, S. (2017). A bioinformatics approach to designing a zika virus vaccine. Computational Biology and Chemistry, 68, 143–152. https://doi.org/10.1016/j.compbiolchem.2017.03.002
  • Diagne, C. T., Bengue, M., Choumet, V., Hamel, R., Pompon, J., & Missé, D. (2020). Mayaro virus pathogenesis and transmission mechanisms. Pathogens, 9(9), 738. https://doi.org/10.3390/pathogens9090738
  • Dimitrov, I., & Doytchinova, I. (2020). An alignment-independent platform for allergenicity prediction. In Immunoinformatics (pp. 147–153). Springer.
  • Dimitrov, I., Bangov, I., Flower, D. R., & Doytchinova, I. (2014). Allertop v.2-a server for in silico prediction of allergens. Journal of Molecular Modeling, 20(6), 2278. https://doi.org/10.1007/s00894-014-2278-5
  • 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
  • Esposito, D. L. A., & Fonseca, BALd. (2017). Will Mayaro virus be responsible for the next outbreak of an arthropod-borne virus in brazil? The Brazilian Journal of Infectious Diseases: An Official Publication of the Brazilian Society of Infectious Diseases, 21(5), 540–544. https://doi.org/10.1016/j.bjid.2017.06.002
  • Figueiredo, MLGd., & Figueiredo, L. T. M. (2014). Emerging alphaviruses in the Americas: Chikungunya and Mayaro. Revista da Sociedade Brasileira de Medicina Tropical, 47(6), 677–683. https://doi.org/10.1590/0037-8682-0246-2014
  • Fleri, W., Paul, S., Dhanda, S. K., Mahajan, S., Xu, X., Peters, B., & Sette, A. (2017). The immune epitope database and analysis resource in epitope discovery and synthetic vaccine design. Frontiers in Immunology, 8, 278. https://doi.org/10.3389/fimmu.2017.00278
  • Gomez de Cedrón, M., Ehsani, N., Mikkola, M. L., García, J. A., & Kääriäinen, L. (1999). RNA helicase activity of semliki forest virus replicase protein nsp2. FEBS Letters, 448(1), 19–22. https://doi.org/10.1016/S0014-5793(99)00321-X
  • González-Galarza, F. F., Takeshita, L. Y. C., Santos, E. J. M., Kempson, F., Maia, M. H. T., da Silva, A. L. S., Teles e Silva, A. L., Ghattaoraya, G. S., Alfirevic, A., Jones, A. R., & Middleton, D. (2015). Allele frequency net 2015 update: New features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Research, 43(Database issue), D784–D788. https://doi.org/10.1093/nar/gku1166
  • Götte, B., Liu, L., & McInerney, G. M. (2018). The enigmatic alphavirus non-structural protein 3 (nsp3) revealing its secrets at last. Viruses, 10(3), 105. https://doi.org/10.3390/v10030105
  • Gupta, S., Kapoor, P., Chaudhary, K., Gautam, A., Kumar, R., & 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
  • Harmalkar, A., & Gray, J. J. (2021). Advances to tackle backbone flexibility in protein docking. Current Opinion in Structural Biology, 67, 178–186. https://doi.org/10.1016/j.sbi.2020.11.011
  • Hassing, R. J., Leparc-Goffart, I., Tolou, H., van Doornum, G., & van Genderen, P. J. (2010). Cross-reactivity of antibodies to viruses belonging to the semliki forest serocomplex. Eurosurveillance, 15(23), 19588. https://doi.org/10.2807/ese.15.23.19588-en
  • Jardine, J., Julien, J.-P., Menis, S., Ota, T., Kalyuzhniy, O., McGuire, A., Sok, D., Huang, P.-S., MacPherson, S., Jones, M., Nieusma, T., Mathison, J., Baker, D., Ward, A. B., Burton, D. R., Stamatatos, L., Nemazee, D., Wilson, I. A., & Schief, W. R. (2013). Rational HIV immunogen design to target specific germline b cell receptors. Science (New York, N.Y.), 340(6133), 711–716. https://doi.org/10.1126/science.1234150
  • Jensen, J. H., Li, H., Robertson, A. D., & Molina, P. A. (2005). Prediction and rationalization of protein pKa values using QM and QM/MM methods. The Journal of Physical Chemistry A, 109(30), 6634–6643. https://doi.org/10.1021/jp051922x
  • Kadam, A., Sasidharan, S., & Saudagar, P. (2020). Computational design of a potential multi-epitope subunit vaccine using immunoinformatics to fight Ebola virus. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 85, 104464. https://doi.org/10.1016/j.meegid.2020.104464
  • Kam, Y.-W., Lum, F.-M., Teo, T.-H., Lee, W. W. L., Simarmata, D., Harjanto, S., Chua, C.-L., Chan, Y.-F., Wee, J.-K., Chow, A., Lin, R. T. P., Leo, Y.-S., Le Grand, R., Sam, I.-C., Tong, J.-C., Roques, P., Wiesmüller, K.-H., Rénia, L., Rötzschke, O., & Ng, L. F. P. (2012). Early neutralizing igg response to chikungunya virus in infected patients targets a dominant linear epitope on the e2 glycoprotein. EMBO Molecular Medicine, 4(4), 330–343. https://doi.org/10.1002/emmm.201200213
  • Khan, S., Khan, A., Rehman, A. U., Ahmad, I., Ullah, S., Khan, A. A., Ali, S. S., Afridi, S. G., & Wei, D.-Q. (2019). Immunoinformatics and structural vaccinology driven prediction of multi-epitope vaccine against Mayaro virus and validation through in-silico expression. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 73, 390–400. https://doi.org/10.1016/j.meegid.2019.06.006
  • Kim, T.-J., Lee, S.-T., Moon, J., Sunwoo, J.-S., Byun, J.-I., Lim, J.-A., Shin, Y.-W., Jun, J.-S., Lee, H. S., Lee, W.-J., Yang, A. R., Choi, Y., Park, K.-I., Jung, K.-H., Jung, K.-Y., Kim, M., Lee, S. K., & Chu, K. (2017). Anti-lgi1 encephalitis is associated with unique HLA subtypes. Annals of Neurology, 81(2), 183–192. https://doi.org/10.1002/ana.24860
  • Kotturi, M. F., Scott, I., Wolfe, T., Peters, B., Sidney, J., Cheroutre, H., von Herrath, M. G., Buchmeier, M. J., Grey, H., & Sette, A. (2008). Naive precursor frequencies and mhc binding rather than the degree of epitope diversity shape cd8+ t cell immunodominance. Journal of Immunology (Baltimore, Md. : 1950), 181(3), 2124–2133. https://doi.org/10.4049/jimmunol.181.3.2124
  • Kumar, S., Mamidi, P., Kumar, A., Basantray, I., Bramha, U., Dixit, A., Maiti, P. K., Singh, S., Suryawanshi, A. R., Chattopadhyay, S., & Chattopadhyay, S. (2015). Development of novel antibodies against non-structural proteins nsp1, nsp3 and nsp4 of chikungunya virus: Potential use in basic research. Archives of Virology, 160(11), 2749–2761. https://doi.org/10.1007/s00705-015-2564-2
  • LaBeaud, A. D. (2008). Why arboviruses can be neglected tropical diseases. PLoS Neglected Tropical Diseases, 2(6), e247. https://doi.org/10.1371/journal.pntd.0000247
  • Laskowski, R. A., Jabłońska, J., Pravda, L., Vařeková, R. S., & Thornton, J. M. (2018). Pdbsum: Structural summaries of PDB entries. Protein Science: A Publication of the Protein Society, 27(1), 129–134. https://doi.org/10.1002/pro.3289
  • LaStarza, M. W., Lemm, J. A., & Rice, C. M. (1994). Genetic analysis of the nsp3 region of sindbis virus: Evidence for roles in minus-strand and subgenomic rna synthesis. Journal of Virology, 68(9), 5781–5791. https://doi.org/10.1128/JVI.68.9.5781-5791.1994
  • Lavergne, A., de Thoisy, B., Lacoste, V., Pascalis, H., Pouliquen, J.-F., Mercier, V., Tolou, H., Dussart, P., Morvan, J., Talarmin, A., & Kazanji, M. (2006). Mayaro virus: Complete nucleotide sequence and phylogenetic relationships with other alphaviruses. Virus Research, 117(2), 283–290. https://doi.org/10.1016/j.virusres.2005.11.006
  • Lednicky, J., De Rochars, V. M. B., Elbadry, M., Loeb, J., Telisma, T., Chavannes, S., Anilis, G., Cella, E., Ciccozzi, M., Okech, B., Salemi, M., & Morris, J. G. (2016). Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases, 22(11), 2000–2002. https://doi.org/10.3201/eid2211.161015
  • Lee, G. R., Won, J., Heo, L., & Seok, C. (2019). Galaxyrefine2: Simultaneous refinement of inaccurate local regions and overall protein structure. Nucleic Acids Research, 47(W1), W451–W455. https://doi.org/10.1093/nar/gkz288
  • 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
  • Ling, Y.-M., Chen, J.-Y., Guo, L., Wang, C.-Y., Tan, W.-T., Wen, Q., Zhang, S.-D., Deng, G.-H., Lin, Y., & Kwok, H. F. (2017). β-defensin 1 expression in HCV infected liver/liver cancer: An important role in protecting HCV progression and liver cancer development. Scientific Reports, 7(1), 1–14. https://doi.org/10.1038/s41598-017-13332-0
  • Lundberg, M. (2009). The oniom method and its applications to enzymatic reactions. In Multi-scale quantum models for biocatalysis (pp. 21–55). Springer.
  • Mackay, I. M., & Arden, K. E. (2016). Mayaro virus: A forest virus primed for a trip to the city? Microbes and Infection, 18(12), 724–734. https://doi.org/10.1016/j.micinf.2016.10.007
  • Malathi, K., & Ramaiah, S. (2018). Bioinformatics approaches for new drug discovery: A review. Biotechnology & Genetic Engineering Reviews, 34(2), 243–260. https://doi.org/10.1080/02648725.2018.1502984
  • Marcondes, C. B., Contigiani, M., & Gleiser, R. M. (2017). Emergent and reemergent arboviruses in South America and the Caribbean: Why so many and why now? Journal of Medical Entomology, 54(3), 509–532. https://doi.org/10.1093/jme/tjw209
  • McKeever, T. M., Lewis, S. A., Smith, C., & Hubbard, R. (2004). Vaccination and allergic disease: A birth cohort study. American Journal of Public Health, 94(6), 985–989. https://doi.org/10.2105/ajph.94.6.985
  • Meshram, C. D., Agback, P., Shiliaev, N., Urakova, N., Mobley, J. A., Agback, T., Frolova, E. I., & Frolov, I. (2018). Multiple host factors interact with the hypervariable domain of chikungunya virus nsp3 and determine viral replication in cell-specific mode. Journal of Virology, 92(16), e00838–18. https://doi.org/10.1128/JVI.00838-18
  • 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), 22. https://doi.org/10.1186/1742-4682-10-22
  • Mittal, A., Sasidharan, S., Raj, S., Balaji, S. N., & Saudagar, P. (2020). Exploring the Zika genome to design a potential multiepitope vaccine using an immunoinformatics approach. International Journal of Peptide Research and Therapeutics, 26(4), 2231–2210. https://doi.org/10.1007/s10989-020-10020-y
  • Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). Autodock4 and autodocktools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
  • Narula, A., Pandey, R. K., Khatoon, N., Mishra, A., & Prajapati, V. K. (2018). Excavating chikungunya genome to design b and t cell multi-epitope subunit vaccine using comprehensive immunoinformatics approach to control chikungunya infection. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 61, 4–15. https://doi.org/10.1016/j.meegid.2018.03.007
  • Nelson, S. A., & Sant, A. J. (2019). Imprinting and editing of the human cd4 t cell response to influenza virus. Frontiers in Immunology, 10, 932. https://doi.org/10.3389/fimmu.2019.00932
  • Nielsen, P. H., Kragelund, C., Seviour, R. J., & Nielsen, J. L. (2009). Identity and ecophysiology of filamentous bacteria in activated sludge. FEMS Microbiology Reviews, 33(6), 969–998. https://doi.org/10.1111/j.1574-6976.2009.00186.x
  • Nielsen, M., Lundegaard, C., Blicher, T., Lamberth, K., Harndahl, M., Justesen, S., Røder, G., Peters, B., Sette, A., Lund, O., & Buus, S. (2007). Netmhcpan, a method for quantitative predictions of peptide binding to any HLA-a and-b locus protein of known sequence. PLoS One, 2(8), e796. https://doi.org/10.1371/journal.pone.0000796
  • Ong, E., He, Y., & Yang, Z. (2020). Epitope promiscuity and population coverage of mycobacterium tuberculosis protein antigens in current subunit vaccines under development. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 80, 104186. https://doi.org/10.1016/j.meegid.2020.104186
  • 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
  • Patronov, A., & Doytchinova, I. (2013). T-cell epitope vaccine design by immunoinformatics. Open Biology, 3(1), 120139. https://doi.org/10.1098/rsob.120139
  • Perales-Linares, R., & Navas-Martin, S. (2013). Toll-like receptor 3 in viral pathogenesis: Friend or foe? Immunology, 140(2), 153–167. https://doi.org/10.1111/imm.12143
  • Peters, B., Bulik, S., Tampe, R., Van Endert, P. M., & Holzhütter, H.-G. (2003). Identifying MHC class I epitopes by predicting the tap transport efficiency of epitope precursors. Journal of Immunology (Baltimore, Md.: 1950), 171(4), 1741–1749. https://doi.org/10.4049/jimmunol.171.4.1741
  • Prat, C. M., Flusin, O., Panella, A., Tenebray, B., Lanciotti, R., & Leparc-Goffart, I. (2014). Evaluation of commercially available serologic diagnostic tests for chikungunya virus. Emerging Infectious Diseases, 20(12), 2129–2132. https://doi.org/10.3201/eid2012.141269
  • Prathyusha, A., Bhukya, P. L., & Bramhachari, P. V. (2020). Potentiality of toll-like receptors (tlrs) in viral infections. In Dynamics of immune activation in viral diseases (pp. 149–159). Springer.
  • Rakib, A., Sami, S. A., Mimi, N. J., Chowdhury, M. M., Eva, T. A., Nainu, F., Paul, A., Shahriar, A., Tareq, A. M., Emon, N. U., Chakraborty, S., Shil, S., Mily, S. J., Ben Hadda, T., Almalki, F. A., & Emran, T. B. (2020). Immunoinformatics-guided design of an epitope-based vaccine against severe acute respiratory syndrome coronavirus 2 spike glycoprotein. Computers in Biology and Medicine, 124, 103967. https://doi.org/10.1016/j.compbiomed.2020.103967
  • Ravichandran, L., Venkatesan, A., & Febin Prabhu Dass, J. (2019). Epitope-based immunoinformatics approach on RNA-dependent RNA polymerase (RDRP) protein complex of Nipah virus (niv). Journal of Cellular Biochemistry, 120(5), 7082–7095. https://doi.org/10.1002/jcb.27979
  • Robinson, D. M., Cole, F. E., McManus, A. T., & Pedersen, C. E. (1976). Inactivated Mayaro vaccine produced in human diploid cell cultures. Military Medicine, 141(3), 163–166. https://doi.org/10.1093/milmed/141.3.163
  • Rodrigues, R. L., Menezes, G. D. L., Saivish, M. V., Costa, V. G. D., Pereira, M., Moreli, M. L., & Silva, R. A. D. (2019). Prediction of Mayv peptide antigens for immunodiagnostic tests by immunoinformatics and molecular dynamics simulations. Scientific Reports, 9(1), 1–10. https://doi.org/10.1038/s41598-019-50008-3
  • 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
  • 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
  • Senn, H. M., & Thiel, W. (2009). Qm/mm methods for biomolecular systems. Angewandte Chemie (International ed. in English), 48(7), 1198–1229. https://doi.org/10.1002/anie.200802019
  • Silva, M. K., Gomes, H. S. S., Silva, O. L. T., Campanelli, S. E., Campos, D. M. O., Araújo, J. M. G., Fernandes, J. V., Fulco, U. L., & Oliveira, J. I. N. (2021). Identification of promiscuous t cell epitopes on Mayaro virus structural proteins using immunoinformatics, molecular modeling, and QM:MM approaches. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 91, 104826. https://doi.org/10.1016/j.meegid.2021.104826
  • Singh, H., & Raghava, G. (2003). Propred1: Prediction of promiscuous MHC class-I binding sites. Bioinformatics (Oxford, England), 19(8), 1009–1014. https://doi.org/10.1093/bioinformatics/btg108
  • Sousa, S. F., Fernandes, P. A., & Ramos, M. J. (2006). Protein-ligand docking: Current status and future challenges. Proteins, 65(1), 15–26. https://doi.org/10.1002/prot.21082
  • Sproviero, E. M., Newcomer, M. B., Gascón, J. A., Batista, E. R., Brudvig, G. W., & Batista, V. S. (2009). The mod-qm/mm methodology for structural refinement of photosystem ii and other biological macromolecules. Photosynthesis Research, 102(2–3), 455–470. https://doi.org/10.1007/s11120-009-9467-6
  • Stryhn, A., Kongsgaard, M., Rasmussen, M., Harndahl, M. N., Østerbye, T., Bassi, M. R., Thybo, S., Gabriel, M., Hansen, M. B., Nielsen, M., Christensen, J. P., Randrup Thomsen, A., & Buus, S. (2020). A Systematic, Unbiased Mapping of CD8+ and CD4+ T Cell Epitopes in Yellow Fever Vaccinees. Frontiers in Immunology, 11, 1836. https://doi.org/10.3389/fimmu.2020.01836
  • Tahir Ul Qamar, M., Saleem, S., Ashfaq, U. A., Bari, A., Anwar, F., & Alqahtani, S. (2019). Epitope-based peptide vaccine design and target site depiction against middle east respiratory syndrome coronavirus: An immune-informatics study. Journal of Translational Medicine, 17(1), 362. https://doi.org/10.1186/s12967-019-2116-8
  • Tomar, S., Hardy, R. W., Smith, J. L., & Kuhn, R. J. (2006). Catalytic core of alphavirus nonstructural protein nsp4 possesses terminal adenylyltransferase activity. Journal of Virology, 80(20), 9962–9969. https://doi.org/10.1128/JVI.01067-06
  • Vasiljeva, L., Valmu, L., Kääriäinen, L., & Merits, A. (2001). Site-specific protease activity of the carboxyl-terminal domain of semliki forest virus replicase protein nsp2. The Journal of Biological Chemistry, 276(33), 30786–30793. https://doi.org/10.1074/jbc.M104786200
  • 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–D412. https://doi.org/10.1093/nar/gku938
  • Waheed, Y., Safi, S. Z., Najmi, M. H., Aziz, H., & Imran, M. (2017). Prediction of promiscuous t cell epitopes in RNA dependent RNA polymerase of chikungunya virus. Asian Pacific Journal of Tropical Medicine, 10(8), 760–764. https://doi.org/10.1016/j.apjtm.2017.07.023
  • Wang, Y. F., Sawicki, S. G., & Sawicki, D. L. (1994). Alphavirus nsp3 functions to form replication complexes transcribing negative-strand RNA. Journal of Virology, 68(10), 6466–6475. https://doi.org/10.1128/JVI.68.10.6466-6475.1994
  • 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
  • Williams, C. J., Headd, J. J., Moriarty, N. W., Prisant, M. G., Videau, L. L., Deis, L. N., Verma, V., Keedy, D. A., Hintze, B. J., Chen, V. B., Jain, S., Lewis, S. M., Arendall, W. B., Snoeyink, J., Adams, P. D., Lovell, S. C., Richardson, J. S., & Richardson, D. C. (2018). Molprobity: More and better reference data for improved all-atom structure validation. Protein Science: A Publication of the Protein Society, 27(1), 293–315. https://doi.org/10.1002/pro.3330
  • Woods, C. J., Manby, F. R., & Mulholland, A. J. (2008). An efficient method for the calculation of quantum mechanics/molecular mechanics free energies. The Journal of Chemical Physics, 128(1), 014109. https://doi.org/10.1063/1.2805379
  • Xu, D., & Zhang, Y. (2012). Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field. Proteins, 80(7), 1715–1735. https://doi.org/10.1002/prot.24065
  • Yazdani, Z., Rafiei, A., Valadan, R., Ashrafi, H., Pasandi, M., & Kardan, M. (2020). Designing a potent l1 protein-based hpv peptide vaccine: A bioinformatics approach. Computational Biology and Chemistry, 85, 107209. https://doi.org/10.1016/j.compbiolchem.2020.107209
  • Zanatta, G., Nunes, G., Bezerra, E. M., da Costa, R. F., Martins, A., Caetano, E. W. S., Freire, V. N., & Gottfried, C. (2014). Antipsychotic haloperidol binding to the human dopamine d3 receptor: Beyond docking through qm/mm refinement toward the design of improved schizophrenia medicines. ACS Chemical Neuroscience, 5(10), 1041–1054. https://doi.org/10.1021/cn500111e
  • Zeidler, J., Fernandes-Siqueira, L., Barbosa, G., & Da Poian, A. (2017). Non-canonical roles of dengue virus non-structural proteins. Viruses, 9(3), 42. https://doi.org/10.3390/v9030042

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.