673
Views
3
CrossRef citations to date
0
Altmetric
Research Article

Development of a novel circular mRNA vaccine of six protein combinations against Staphylococcus aureus

, , , , , , , , , & show all
Pages 10525-10545 | Received 22 Aug 2022, Accepted 29 Nov 2022, Published online: 19 Dec 2022

References

  • Abbas, A. K., Trotta, E. D. R. S., Marson, A., & Bluestone, J. A. (2018). Revisiting IL-2: Biology and therapeutic prospects. Science Immunology, 25, 3. https://doi.org/10.1126/sciimmunol.aat1482
  • 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
  • Alfeo, M. J., Pagotto, A., Barbieri, G., Foster, T. J., Vanhoorelbeke, K., De Filippis, V., Speziale, P., & Pietrocola, G. (2021). Staphylococcus aureus iron-regulated surface determinant B (IsdB) protein interacts with von Willebrand factor and promotes adherence to endothelial cells. Scientific Reports, 11(1), 22799. https://doi.org/10.1038/s41598-021-02065-w
  • Antimicrobial Resistance. (2022). Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. The Lancet, 399(10325), 629–655. https://doi.org/10.1016/S0140-6736(21)02724-0
  • Baek, M., DiMaio, F., Anishchenko, I., Dauparas, J., Ovchinnikov, S., Lee, G. R., Wang, J., Cong, Q., Kinch, L. N., Schaeffer, R. D., Millán, C., Park, H., Adams, C., Glassman, C. R., DeGiovanni, A., Pereira, J. H., Rodrigues, A. V., van Dijk, A. A., Ebrecht, A. C., … Baker, D. (2021). Accurate prediction of protein structures and interactions using a three-track neural network. Science (New York, N.Y.), 373(6557), 871–876. https://doi.org/10.1126/science.abj8754
  • 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, 25(6), 1316–1327. https://doi.org/10.1016/j.ymthe.2017.03.035
  • Begier, E., Seiden, D. J., Patton, M., Zito, E., Severs, J., Cooper, D., Eiden, J., Gruber, W. C., Jansen, K. U., Anderson, A. S., & Gurtman, A. (2017). SA4Ag, a 4-antigen Staphylococcus aureus vaccine, rapidly induces high levels of bacteria-killing antibodies. Vaccine, 35(8), 1132–1139. https://doi.org/10.1016/j.vaccine.2017.01.024
  • 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. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
  • 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
  • Cabrera, R., Fernández-Barat, L., Motos, A., López-Aladid, R., Vázquez, N., Panigada, M., Álvarez-Lerma, F., López, Y., Muñoz, L., Castro, P., Vila, J., & Torres, A. (2020). Molecular characterization of methicillin-resistant Staphylococcus aureus clinical strains from the endotracheal tubes of patients with nosocomial pneumonia. Antimicrobial Resistance and Infection Control, 9(1), 43. https://doi.org/10.1186/s13756-020-0679-z
  • Calis, J. J. A., 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
  • Chambers, H. F., & Deleo, F. R. (2009). Waves of resistance: Staphylococcus aureus in the antibiotic era. Nature Reviews. Microbiology, 7(9), 629–641. https://doi.org/10.1038/nrmicro2200
  • Chauhan, V., Rungta, T., Rawat, M., Goyal, K., Gupta, Y., & Singh, M. P. (2021). Excavating SARS-coronavirus 2 genome for epitope-based subunit vaccine synthesis using immunoinformatics approach. Journal of Cellular Physiology, 236(2), 1131–1147. https://doi.org/10.1002/jcp.29923
  • Chen, C., Li, Z., Huang, H., Suzek, B. E., Wu, C. H., & UniProt, C. (2013). A fast peptide match service for UniProt knowledgebase. Bioinformatics (Oxford, England), 29(21), 2808–2809. https://doi.org/10.1093/bioinformatics/btt484
  • Cohen, I., Coban, M., Shahar, A., Sankaran, B., Hockla, A., Lacham, S., Caulfield, T. R., Radisky, E. S., & Papo, N. (2019). Disulfide engineering of human Kunitz-type serine protease inhibitors enhances proteolytic stability and target affinity toward mesotrypsin. The Journal of Biological Chemistry, 294(13), 5105–5120. https://doi.org/10.1074/jbc.RA118.007292
  • Corbett, K. S., Edwards, D. K., Leist, S. R., Abiona, O. M., Boyoglu-Barnum, S., Gillespie, R. A., Himansu, S., Schäfer, A., Ziwawo, C. T., DiPiazza, A. T., Dinnon, K. H., Elbashir, S. M., Shaw, C. A., Woods, A., Fritch, E. J., Martinez, D. R., Bock, K. W., Minai, M., Nagata, B. M., … Graham, B. S. (2020). SARS-CoV-2 mRNA vaccine design enabled by prototype pathogen preparedness. Nature, 586(7830), 567–571. https://doi.org/10.1038/s41586-020-2622-0
  • 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
  • Dalla Serra, M., Coraiola, M., Viero, G., Comai, M., Potrich, C., Ferreras, M., Baba-Moussa, L., Colin, D. A., Menestrina, G., Bhakdi, S., & Prévost, G. (2005). Staphylococcus aureus bicomponent gamma-hemolysins, HlgA, HlgB, and HlgC, can form mixed pores containing all components. Journal of Chemical Information and Modelling, 45(6), 1539–1545. https://doi.org/10.1021/ci050175y
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: AnN⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
  • Dey, J., Mahapatra, S. R., Lata, S., Patro, S., Misra, N., & Suar, M. (2022). Exploring Klebsiella pneumoniae capsule polysaccharide proteins to design multiepitope subunit vaccine to fight against pneumonia. Expert Review of Vaccines, 21(4), 569–587. https://doi.org/10.1080/14760584.2022.2021882
  • Dey, J., Mahapatra, S. R., Patnaik, S., Lata, S., Kushwaha, G. S., Panda, R. K., Misra, N., & Suar, M. (2022). Molecular characterization and designing of a novel multiepitope vaccine construct against Pseudomonas aeruginosa. International Journal of Peptide Research and Therapeutics, 28(2), 49. https://doi.org/10.1007/s10989-021-10356-z
  • Dey, J., Mahapatra, S. R., Raj, T. K., Kaur, T., Jain, P., Tiwari, A., Patro, S., Misra, N., & Suar, M. (2022). Designing a novel multi-epitope vaccine to evoke a robust immune response against pathogenic multidrug-resistant Enterococcus faecium bacterium. Gut Pathogens, 14(1), 21. https://doi.org/10.1186/s13099-022-00495-z
  • Dey, J., Mahapatra, S. R., Singh, P., Patro, S., Kushwaha, G. S., Misra, N., & Suar, M. (2021). B and T cell epitope-based peptides predicted from clumping factor protein of Staphylococcus aureus as vaccine targets. Microbial Pathogenesis, 160, 105171. https://doi.org/10.1016/j.micpath.2021.105171
  • 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
  • Dhanda, S. K., Vir, P., & Raghava, G. P. (2013). Designing of interferon-gamma inducing MHC class-II binders. Biology Direct, 8(1), 30. https://doi.org/10.1186/1745-6150-8-30
  • Dimitrov, I., Bangov, I., Flower, D. R., & Doytchinova, I. (2014). AllerTOP v.2–a server for in silico prediction of allergens. Journal of Molecular Modelling, 20(6), 2278. https://doi.org/10.1007/s00894-014-2278-5
  • Dombkowski, A. A., Sultana, K. Z., & Craig, D. B. (2014). Protein disulfide engineering. FEBS Letters, 588(2), 206–212. https://doi.org/10.1016/j.febslet.2013.11.024
  • 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
  • Edwards, A. M., Potts, J. R., Josefsson, E., & Massey, R. C. (2010). Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathogens, 6(6), e1000964. https://doi.org/10.1371/journal.ppat.1000964
  • Ford, E., & Ares, M. Jr. (1994). Synthesis of circular RNA in bacteria and yeast using RNA cyclase ribozymes derived from a group I intron of phage T4. Proceedings of the National Academy of Sciences of the United States of America, 91(8), 3117–3121. https://doi.org/10.1073/pnas.91.8.3117
  • Francois, B., Mercier, E., Gonzalez, C., Asehnoune, K., Nseir, S., Fiancette, M., Desachy, A., Plantefève, G., Meziani, F., de Lame, P.-A., & Laterre, P.-F. (2018). Safety and tolerability of a single administration of AR-301, a human monoclonal antibody, in ICU patients with severe pneumonia caused by Staphylococcus aureus: first-in-human trial. Intensive Care Medicine, 44(11), 1787–1796. https://doi.org/10.1007/s00134-018-5229-2
  • Frenck, R. W., Creech, C. B., Sheldon, E. A., Seiden, D. J., Kankam, M. K., Baber, J., Zito, E., Hubler, R., Eiden, J., Severs, J. M., Sebastian, S., Nanra, J., Jansen, K. U., Gruber, W. C., Anderson, A. S., & Girgenti, D. (2017). Safety, tolerability, and immunogenicity of a 4-antigen Staphylococcus aureus vaccine (SA4Ag): Results from a first-in-human randomised, placebo-controlled phase 1/2 study. Vaccine, 35(2), 375–384. https://doi.org/10.1016/j.vaccine.2016.11.010
  • Geriak, M., Haddad, F., Rizvi, K., Rose, W., Kullar, R., LaPlante, K., Yu, M., Vasina, L., Ouellette, K., Zervos, M., Nizet, V., & Sakoulas, G. (2019). Clinical data on daptomycin plus ceftaroline versus standard of care monotherapy in the treatment of methicillin-resistant Staphylococcus aureus bacteremia. Antimicrobial Agents and Chemotherapy, 63(5), e02483-18. https://doi.org/10.1128/AAC.02483-18
  • Gianquinto, E., Moscetti, I., De Bei, O., Campanini, B., Marchetti, M., Luque, F. J., Cannistraro, S., Ronda, L., Bizzarri, A. R., Spyrakis, F., & Bettati, S. (2019). Interaction of human hemoglobin and semi-hemoglobins with the Staphylococcus aureus hemophore IsdB: A kinetic and mechanistic insight. Scientific Reports, 9(1), 18629. https://doi.org/10.1038/s41598-019-54970-w
  • Graille, M., Stura, E. A., Corper, A. L., Sutton, B. J., Taussig, M. J., Charbonnier, J. B., & Silverman, G. J. (2000). Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: Structural basis for recognition of B-cell receptors and superantigen activity. Proceedings of the National Academy of Sciences of the United States of America, 97(10), 5399–5404. https://doi.org/10.1073/pnas.97.10.5399
  • Grote, A., Hiller, K., Scheer, M., Munch, R., Nortemann, 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(Web Server issue), W526–531. https://doi.org/10.1093/nar/gki376
  • Guo, Y., Song, G., Sun, M., Wang, J., & Wang, Y. (2020). Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Frontiers in Cellular and Infection Microbiology, 10, 107. https://doi.org/10.3389/fcimb.2020.00107
  • Gupta, S., Kapoor, P., Chaudhary, K., Gautam, A., Kumar, R., Open Source Drug Discovery, C., & Raghava, G. P. (2013). In silico approach for predicting toxicity of peptides and proteins. PLoS One, 8(9), e73957. https://doi.org/10.1371/journal.pone.0073957
  • Hallgren, J., Tsirigos, K. D., Pedersen, M. D., Almagro Armenteros, J. J., Marcatili, P., Nielsen, H., Krogh, A., & Winther, O. (2022). DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. https://doi.org/10.1101/2022.04.08.487609
  • Hess, B. (2008). P-LINCS: A parallel linear constraint solver for molecular simulation. Journal of Chemical Theory and Computation, 4(1), 116–122. https://doi.org/10.1021/ct700200b
  • Hussain, S., Joo, J., Kang, J., Kim, B., Braun, G. B., She, Z.-G., Kim, D., Mann, A. P., Mölder, T., Teesalu, T., Carnazza, S., Guglielmino, S., Sailor, M. J., & Ruoslahti, E. (2018). Antibiotic-loaded nanoparticles targeted to the site of infection enhance antibacterial efficacy. Nature Biomedical Engineering, 2(2), 95–103. https://doi.org/10.1038/s41551-017-0187-5
  • Hussain, M., Kohler, C., & Becker, K. (2022). Enolase of Staphylococcus lugdunensis is a surface-exposed moonlighting protein that binds to extracellular matrix and the plasminogen/plasmin system. Frontiers in Microbiology, 13, 837297. https://doi.org/10.3389/fmicb.2022.837297
  • Jespersen, M. C., Peters, B., Nielsen, M., & Marcatili, P. (2017). BepiPred-2.0: Improving sequence-based B-cell epitope prediction using conformational epitopes. Nucleic Acids Research, 45(W1), W24–W29. https://doi.org/10.1093/nar/gkx346
  • Jun, S. Y., Jang, I. J., Yoon, S., Jang, K., Yu, K.-S., Cho, J. Y., Seong, M.-W., Jung, G. M., Yoon, S. J., & Kang, S. H. (2017). Pharmacokinetics and tolerance of the phage endolysin-based candidate drug SAL200 after a single intravenous administration among healthy volunteers. Antimicrobial Agents and Chemotherapy, 61(6), e02629-16. https://doi.org/10.1128/AAC.02629-16
  • Junttila, I. S. (2018). Tuning the cytokine responses: An update on interleukin (IL)-4 and IL-13 receptor complexes. Frontiers in Immunology, 9, 888. https://doi.org/10.3389/fimmu.2018.00888
  • Kak, G., Raza, M., & Tiwari, B. K. (2018). Interferon-gamma (IFN-gamma): Exploring its implications in infectious diseases. Biomolecular Concepts, 9(1), 64–79. https://doi.org/10.1515/bmc-2018-0007
  • Khan, S., Shaker, B., Ahmad, S., Abbasi, S. W., Arshad, M., Haleem, A., Ismail, S., Zaib, A., & Sajjad, W. (2021). Towards a novel peptide vaccine for Middle East respiratory syndrome coronavirus and its possible use against pandemic COVID-19. Journal of Molecular Liquids, 324, 114706. https://doi.org/10.1016/j.molliq.2020.114706
  • Khodadadi, M., Ghaffarifar, F., Dalimi, A., & Ahmadpour, E. (2021). Immunogenicity of in-silico designed multi-epitope DNA vaccine encoding SAG1, SAG3 and SAG5 of Toxoplasma gondii adjuvanted with CpG-ODN against acute toxoplasmosis in BALB/c mice. Acta Tropica, 216, 105836. https://doi.org/10.1016/j.actatropica.2021.105836
  • Kim, S. C., Sekhon, S. S., Shin, W. R., Ahn, G., Cho, B. K., Ahn, J. Y., & Kim, Y. H. (2022). Modifications of mRNA vaccine structural elements for improving mRNA stability and translation efficiency. Molecular & Cellular Toxicology, 18(1), 1–8. https://doi.org/10.1007/s13273-021-00171-4
  • Ko, J., Park, H., Heo, L., & Seok, C. (2012). GalaxyWEB server for protein structure prediction and refinement. Nucleic Acids Research, 40(Web Server issue), W294–297. https://doi.org/10.1093/nar/gks493
  • 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
  • Kou, Y., Xu, Y., Zhao, Z., Liu, J., Wu, Y., You, Q., Wang, L., Gao, F., Cai, L., & Jiang, C. (2017). Tissue plasminogen activator (tPA) signal sequence enhances immunogenicity of MVA-based vaccine against tuberculosis. Immunology Letters, 190, 51–57. https://doi.org/10.1016/j.imlet.2017.07.007
  • Krautler, N. J., Suan, D., Butt, D., Bourne, K., Hermes, J. R., Chan, T. D., Sundling, C., Kaplan, W., Schofield, P., Jackson, J., Basten, A., Christ, D., & Brink, R. (2017). Differentiation of germinal centre B cells into plasma cells is initiated by high-affinity antigen and completed by Tfh cells. The Journal of Experimental Medicine, 214(5), 1259–1267. https://doi.org/10.1084/jem.20161533
  • 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 (Baltimore, Md. : 1950), 180(1), 309–318. https://doi.org/10.4049/jimmunol.180.1.309
  • Kurcinski, M., Jamroz, M., Blaszczyk, M., Kolinski, A., & Kmiecik, S. (2015). CABS-dock web server for the flexible docking of peptides to proteins without prior knowledge of the binding site. Nucleic Acids Research, 43(W1), W419–424. https://doi.org/10.1093/nar/gkv456
  • Lamiable, A., Thevenet, P., Rey, J., Vavrusa, M., Derreumaux, P., & Tuffery, P. (2016). PEP-FOLD3: Faster de novo structure prediction for linear peptides in solution and in complex. Nucleic Acids Research, 44(W1), W449–454. https://doi.org/10.1093/nar/gkw329
  • 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(1), 424. https://doi.org/10.1186/1471-2105-8-424
  • Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., & Thornton, J. M. (1996). AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. Journal of Biomolecular NMR, 8(4), 477–486. https://doi.org/10.1007/BF00228148
  • Li, G., Huang, Z., Zhang, C., Dong, B.-J., Guo, R.-H., Yue, H.-W., Yan, L.-T., & Xing, X.-H. (2016). Construction of a linker library with widely controllable flexibility for fusion protein design. Applied Microbiology and Biotechnology, 100(1), 215–225. https://doi.org/10.1007/s00253-015-6985-3
  • 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
  • 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
  • Liu, X., Zhang, Y., Zhou, S., Dain, L., Mei, L., & Zhu, G. (2022). Circular RNA: An emerging frontier in RNA therapeutic targets, RNA therapeutics, and mRNA vaccines. Journal of Controlled Release, 348, 84–94. https://doi.org/10.1016/j.jconrel.2022.05.043
  • Livingston, B., Crimi, C., Newman, M., Higashimoto, Y., Appella, E., Sidney, J., & Sette, A. (2002). A rational strategy to design multiepitope immunogens based on multiple Th lymphocyte epitopes. Journal of Immunology (Baltimore, Md.: 1950), 168(11), 5499–5506. https://doi.org/10.4049/jimmunol.168.11.5499
  • Lopez-Blanco, J. R., Aliaga, J. I., Quintana-Orti, E. S., & Chacon, P. (2014). iMODS: Internal coordinates normal mode analysis server. Nucleic Acids Research, 42(Web Server issue), W271–276. https://doi.org/10.1093/nar/gku339
  • Madeira, F., Pearce, M., Tivey, A. R. N., Basutkar, P., Lee, J., Edbali, O., … Lopez, R. (2022). Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Research, 50(W1), W276–9. https://doi.org/10.1093/nar/gkac240
  • Mahapatra, S. R., Dey, J., Jaiswal, A., Roy, R., Misra, N., & Suar, M. (2022). Immunoinformatics-guided designing of epitope-based subunit vaccine from Pilus assembly protein of Acinetobacter baumannii bacteria. Journal of Immunological Methods, 508, 113325. https://doi.org/10.1016/j.jim.2022.113325
  • Mahapatra, S. R., Dey, J., Kushwaha, G. S., Puhan, P., Mohakud, N. K., Panda, S. K., Lata, S., Misra, N., & Suar, M. (2021). Immunoinformatic approach employing modelling and simulation to design a novel vaccine construct targeting MDR efflux pumps to confer wide protection against typhoidal Salmonella serovars. Journal of Biomolecular Structure and Dynamics, 1–13. https://doi.org/10.1080/07391102.2021.1964600
  • Mahapatra, S. R., Dey, J., Raj, T. K., Kumar, V., Ghosh, M., Verma, K. K., Kaur, T., Kesawat, M. S., Misra, N., & Suar, M. (2022). The potential of plant-derived secondary metabolites as novel drug candidates against Klebsiella pneumoniae: Molecular docking and simulation investigation. South African Journal of Botany, 149, 789–797. https://doi.org/10.1016/j.sajb.2022.04.043
  • Mele, T., & Madrenas, J. (2010). TLR2 signalling: At the crossroads of commensalism, invasive infections and toxic shock syndrome by Staphylococcus aureus. The International Journal of Biochemistry & Cell Biology, 42(7), 1066–1071. https://doi.org/10.1016/j.biocel.2010.03.021
  • Meyer, F., Girardot, R., Piemont, Y., Prevost, G., & Colin, D. A. (2009). Analysis of the specificity of panton-valentine leucocidin and gamma-hemolysin F component binding. Infection and Immunity, 77(1), 266–273. https://doi.org/10.1128/IAI.00402-08
  • Miller, L. S., Fowler, V. G., Shukla, S. K., Rose, W. E., & Proctor, R. A. (2020). Development of a vaccine against Staphylococcus aureus invasive infections: Evidence based on human immunity, genetics and bacterial evasion mechanisms. FEMS Microbiology Reviews, 44(1), 123–153. https://doi.org/10.1093/femsre/fuz030
  • 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
  • Narang, P. K., Dey, J., Mahapatra, S. R., Ghosh, M., Misra, N., Suar, M., Kumar, V., & Raina, V. (2021a). Functional annotation and sequence-structure characterization of a hypothetical protein putatively involved in carotenoid biosynthesis in microalgae. South African Journal of Botany, 141, 219–226. https://doi.org/10.1016/j.sajb.2021.04.014
  • Narang, P. K., Dey, J., Mahapatra, S. R., Roy, R., Kushwaha, G. S., Misra, N., Suar, M., & Raina, V. (2021b). Genome-based identification and comparative analysis of enzymes for carotenoid biosynthesis in microalgae. World Journal of Microbiology & Biotechnology, 38(1), 8. https://doi.org/10.1007/s11274-021-03188-y
  • Olson, R., Nariya, H., Yokota, K., Kamio, Y., & Gouaux, E. (1999). Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nature Structural Biology, 6(2), 134–140. https://doi.org/10.1038/5821
  • Parrinello, M., & Rahman, A. (1982). Strain fluctuations and elastic constants. The Journal of Chemical Physics, 76(5), 2662–2666. https://doi.org/10.1063/1.443248
  • Paul, S., Sidney, J., Sette, A., & Peters, B. (2016). TepiTool: A pipeline for computational prediction of T cell epitope candidates. Current Protocols in Immunology, 114, 18.19.1–18.19.24. https://doi.org/10.1002/cpim.12
  • Peck, M., Rothenberg, M. E., Deng, R., Lewin-Koh, N., She, G., Kamath, A. V., Carrasco-Triguero, M., Saad, O., Castro, A., Teufel, L., Dickerson, D. S., Leonardelli, M., & Tavel, J. A. (2019). A Phase 1, randomized, single-ascending-dose study to investigate the safety, tolerability, and pharmacokinetics of DSTA4637S, an anti-Staphylococcus aureus thiomab antibody-antibiotic conjugate, in healthy volunteers. Antimicrobial Agents and Chemotherapy, 63(6), e02588-18. https://doi.org/10.1128/AAC.02588-18
  • Polack, F. P., Thomas, S. J., Kitchin, N., Absalon, J., Gurtman, A., Lockhart, S., Perez, J. L., Pérez Marc, G., Moreira, E. D., Zerbini, C., Bailey, R., Swanson, K. A., Roychoudhury, S., Koury, K., Li, P., Kalina, W. V., Cooper, D., Frenck, R. W., Hammitt, L. L., … Gruber, W. C. (2020). Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. The New England Journal of Medicine, 383(27), 2603–2615. https://doi.org/10.1056/NEJMoa2034577
  • Pollard, A. J., Perrett, K. P., & Beverley, P. C. (2009). Maintaining protection against invasive bacteria with protein-polysaccharide conjugate vaccines. Nature Reviews. Immunology, 9(3), 213–220. https://doi.org/10.1038/nri2494
  • 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, 514. https://doi.org/10.1186/1471-2105-9-514
  • Puttaraju, M., & Been, M. D. (1992). Group I permuted intron-exon (PIE) sequences self-splice to produce circular exons. Nucleic Acids Research, 20(20), 5357–5364. https://doi.org/10.1093/nar/20.20.5357
  • Qu, L., Yi, Z., Shen, Y., Lin, L., Chen, F., Xu, Y., Wu, Z., Tang, H., Zhang, X., Tian, F., Wang, C., Xiao, X., Dong, X., Guo, L., Lu, S., Yang, C., Tang, C., Yang, Y., Yu, W., … Wei, W. (2022). Circular RNA vaccines against SARS-CoV-2 and emerging variants. Cell, 185(10), 1728–1744.e16. https://doi.org/10.1016/j.cell.2022.03.044
  • 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
  • Reynisson, B., Barra, C., Kaabinejadian, S., Hildebrand, W. H., Peters, B., & Nielsen, M. (2020). Improved prediction of MHC II antigen presentation through integration and motif deconvolution of mass spectrometry MHC eluted ligand data. Journal of Proteome Research, 19(6), 2304–2315. https://doi.org/10.1021/acs.jproteome.9b00874
  • 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. e1110. https://doi.org/10.1016/j.cell.2017.02.017
  • Rigi, G., Ghaedmohammadi, S., & Ahmadian, G. (2019). A comprehensive review on staphylococcal protein A (SpA): Its production and applications. Biotechnology and Applied Biochemistry, 66(3), 454–464. https://doi.org/10.1002/bab.1742
  • 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
  • Sakr, A., Bregeon, F., Mege, J. L., Rolain, J. M., & Blin, O. (2018). Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections. Frontiers in Microbiology, 9, 2419. https://doi.org/10.3389/fmicb.2018.02419
  • Sapay, N., Guermeur, Y., & Deleage, G. (2006). Prediction of amphipathic in-plane membrane anchors in monotopic proteins using a SVM classifier. BMC Bioinformatics, 7, 255. https://doi.org/10.1186/1471-2105-7-255
  • Schmidt, C. S., White, C. J., Ibrahim, A. S., Filler, S. G., Fu, Y., Yeaman, M. R., Edwards, J. E., & Hennessey, J. P. Jr. (2012). NDV-3, a recombinant alum-adjuvanted vaccine for Candida and Staphylococcus aureus, is safe and immunogenic in healthy adults. Vaccine, 30(52), 7594–7600. https://doi.org/10.1016/j.vaccine.2012.10.038
  • Shang, W., Hu, Q., Yuan, W., Cheng, H., Yang, J., Hu, Z., Yuan, J., Zhang, X., Peng, H., Yang, Y., Hu, X., Li, M., Zhu, J., & Rao, X. (2016). Comparative fitness and determinants for the characteristic drug resistance of ST239-MRSA-III-t030 and ST239-MRSA-III-t037 strains isolated in China. Microbial Drug Resistance (Larchmont, N.Y.), 22(3), 185–192. https://doi.org/10.1089/mdr.2015.0226
  • Sharma, N., Patiyal, S., Dhall, A., Pande, A., Arora, C., & Raghava, G. P. S. (2021). AlgPred 2.0: An improved method for predicting allergenic proteins and mapping of IgE epitopes. Brief Bioinform, 22(4), bbaa294. https://doi.org/10.1093/bib/bbaa294
  • Sinha, B., François, P. P., Nüsse, O., Foti, M., Hartford, O. M., Vaudaux, P., Foster, T. J., Lew, D. P., Herrmann, M., & Krause, K. H. (1999). Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cellular Microbiology, 1(2), 101–117. https://doi.org/10.1046/j.1462-5822.1999.00011.x
  • Szabo, G. T., Mahiny, A. J., & Vlatkovic, I. (2022). COVID-19 mRNA vaccines: Platforms and current developments. Molecular Therapy, 30(5), 1850–1868. https://doi.org/10.1016/j.ymthe.2022.02.016
  • Tahir Ul Qamar, M., Ahmad, S., Fatima, I., Ahmad, F., Shahid, F., Naz, A., Abbasi, S. W., Khan, A., Mirza, M. U., Ashfaq, U. A., & Chen, L.-L. (2021). Designing multi-epitope vaccine against Staphylococcus aureus by employing subtractive proteomics, reverse vaccinology and immuno-informatics approaches. Computers in Biology and Medicine, 132, 104389. https://doi.org/10.1016/j.compbiomed.2021.104389
  • Tarrahimofrad, H., Rahimnahal, S., Zamani, J., Jahangirian, E., & Aminzadeh, S. (2021). Designing a multi-epitope vaccine to provoke the robust immune response against influenza A H7N9. Scientific Reports, 11(1), 24485. https://doi.org/10.1038/s41598-021-03932-2
  • Teufel, F., Almagro Armenteros, J. J., Johansen, A. R., Gíslason, M. H., Pihl, S. I., Tsirigos, K. D., Winther, O., Brunak, S., von Heijne, G., & Nielsen, H. (2022). SignalP 6.0 predicts all five types of signal peptides using protein language models. Nature Biotechnology, 40(7), 1023–1025. https://doi.org/10.1038/s41587-021-01156-3
  • Thess, A., Grund, S., Mui, B. L., Hope, M. J., Baumhof, P., Fotin-Mleczek, M., & Schlake, T. (2015). Sequence-engineered mRNA without chemical nucleoside modifications enables an effective protein therapy in large animals. Molecular Therapy, 23(9), 1456–1464. https://doi.org/10.1038/mt.2015.103
  • Tomlinson, B. R., Malof, M. E., & Shaw, L. N. (2021). A global transcriptomic analysis of Staphylococcus aureus biofilm formation across diverse clonal lineages. Microbial Genomics, 7(7). https://doi.org/10.1099/mgen.0.000598
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
  • van Zundert, G. C. P., Rodrigues, J. P. G. L. M., Trellet, M., Schmitz, C., Kastritis, P. L., Karaca, E., Melquiond, A. S. J., van Dijk, M., de Vries, S. J., & Bonvin, A. M. J. J. (2016). The HADDOCK2.2 Web Server: User-Friendly Integrative Modelling of Biomolecular Complexes. Journal of Molecular Biology, 428(4), 720–725. https://doi.org/10.1016/j.jmb.2015.09.014
  • Waman, V. P., Sen, N., Varadi, M., Daina, A., Wodak, S. J., Zoete, V., Velankar, S., & Orengo, C. (2021). The impact of structural bioinformatics tools and resources on SARS-CoV-2 research and therapeutic strategies. Briefings in Bioinformatics, 22(2), 742–768. https://doi.org/10.1093/bib/bbaa362
  • Wang, X., Wang, C., Wu, M., Tian, T., Cheng, T., Zhang, X., & Zang, J. (2017). Enolase binds to RnpA in competition with PNPase in Staphylococcus aureus. FEBS Letters, 591(21), 3523–3535. https://doi.org/10.1002/1873-3468.12859
  • Wang, Y., Zhang, Z., Luo, J., Han, X., Wei, Y., & Wei, X. (2021). mRNA vaccine: A potential therapeutic strategy. Molecular Cancer, 20(1), 33. https://doi.org/10.1186/s12943-021-01311-z
  • Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427
  • Wesselhoeft, R. A., Kowalski, P. S., & Anderson, D. G. (2018). Engineering circular RNA for potent and stable translation in eukaryotic cells. Nature Communications, 9(1), 2629. https://doi.org/10.1038/s41467-018-05096-6
  • Wesselhoeft, R. A., Kowalski, P. S., Parker-Hale, F. C., Huang, Y., Bisaria, N., & Anderson, D. G. (2019). RNA circularization diminishes immunogenicity and can extend translation duration in vivo. Molecular Cell, 74(3), 508–520.e4. e504. https://doi.org/10.1016/j.molcel.2019.02.015
  • 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
  • Williams, R. E., Jevons, M. P., Shooter, R. A., Hunter, C. J., Girling, J. A., Griffiths, J. D., & Taylor, G. W. (1959). Nasal staphylococci and sepsis in hospital patients. British Medical Journal, 2(5153), 658–662. https://doi.org/10.1136/bmj.2.5153.658
  • Xu, Z., Shi, L., Wang, Y., Zhang, J., Huang, L., Zhang, C., Liu, S., Zhao, P., Liu, H., Zhu, L., Tai, Y., Bai, C., Gao, T., Song, J., Xia, P., Dong, J., Zhao, J., & Wang, F.-S. (2020). Pathological findings of COVID-19 associated with acute respiratory distress syndrome. The Lancet. Respiratory Medicine, 8(4), 420–422. https://doi.org/10.1016/S2213-2600(20)30076-X
  • Xu, S., Yang, K., Li, R., & Zhang, L. (2020). mRNA vaccine era-mechanisms, drug platform and clinical prospection. International Journal of Molecular Sciences, 21(18), 6582. https://doi.org/10.3390/ijms21186582
  • Yoshitani, J., Kabata, T., Arakawa, H., Kato, Y., Nojima, T., Hayashi, K., Tokoro, M., Sugimoto, N., Kajino, Y., Inoue, D., Ueoka, K., Yamamuro, Y., & Tsuchiya, H. (2020). Combinational therapy with antibiotics and antibiotic-loaded adipose-derived stem cells reduce abscess formation in implant-related infection in rats. Scientific Reports, 10(1), 11182. https://doi.org/10.1038/s41598-020-68184-y
  • Zeng, H., Yang, F., Feng, Q., Zhang, J., Gu, J., Jing, H., Cai, C., Xu, L., Yang, X., Xia, X., Zeng, N., Fan, S., & Zou, Q. (2020). Rapid and broad immune efficacy of a recombinant five-antigen vaccine against Staphylococcus Aureus infection in animal models. Vaccines (Basel), 8(1), 134. https://doi.org/10.3390/vaccines8010134

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.