PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

 

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ISSN 1511-3701

Home / Regular Issue / JTAS Vol. 46 (1) Feb. 2023 / JTAS-2540-2022

 

Characterisation of the Putative Antigenic Genes of the Outer Membrane Proteins of Pasteurella multocida B:2 Strain PMTB2.1 through in silico Analysis

Tahera Hashimi, Deborah Joyce, Sufia Mohd Nasir, Mas Jaffri Masarudin, Annas Salleh and Siti Sarah Othman

Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 1, February 2023

DOI: https://doi.org/10.47836/pjtas.46.1.16

Keywords: Antigenic OMPs, hemorrhagic septicemia, homology modelling, outer membrane proteins, Pasteurella multocida

Published on: 22 Febuary 2023

Outer membrane proteins (OMPs), usually found in Gram-negative bacteria, have long been shown to elicit immune responses in infected hosts. This tendency of OMPs to generate immune reactions makes them ideal candidates for vaccine development against pathogenic bacteria. Pasteurella multocida is a Gram-negative pathogen responsible for the economically significant veterinary disease, hemorrhagic septicemia (HS). HS is an endemic and highly fatal disease affecting buffaloes and cattle. In Malaysia, outbreaks of this disease cost about half a million USD each year. Thus, despite current treatment and prevention measures, HS is a prevalent issue that needs to be overcome. Pasteurella multocida subsp. multocida PMTB2.1, a Malaysian strain of the pathogen, has recently had its entire genome sequenced after being isolated from HS outbreaks in the region. Antigenic OMPs from this strain have since been identified and published for further characterisation. LptD, Wza, and TbpA are integral membrane proteins, while Pal is a peripheral membrane protein that has not been characterised in-depth. This study, therefore, aims to analyse these OMPs through in silico methods. First, protein homology modelling was performed using SWISS-MODEL, whereafter, the structures generated were validated using the SWISS-MODEL structure assessment page, PROCHECK, ERRAT, and PROSA programs. The Pal, Wza, and TbpA structures were good models, while the LptD structure was found to be a near-good model based on the validation performed. Analyses using BCPREDS, NetMHCpan4.1, and NetBoLAIIpan1.0 revealed that these four OMPs could potentially elicit humoral and cellular immune responses.

  • Agrawal, P., Thakur, Z., & Kulharia, M. (2013). Homology modelling and structural validation of tissue factor pathway inhibitor. Bioinformation, 9(16), 808-812. https://doi.org/10.6026/97320630009808

  • Ahmad, T. A., Eweida, A. E., & El-Sayed, L. H. (2016). T-cell epitope mapping for the design of powerful vaccines. Vaccine Reports, 6, 13-22. https://doi.org/10.1016/j.vacrep.2016.07.002

  • Al-Hasani, K., Boyce, J., McCarl, V. P., Bottomley, S., Wilkie, I., & Adler, B. (2007). Identification of novel immunogens in Pasteurella multocida. Microbial Cell Factories, 6, 3. https://doi.org/10.1186/1475-2859-6-3

  • Arévalo‐Herrera, M., Valencia, A. Z., Vergara, J., Bonelo, A., Fleischhauer, K., González, J. M., Restrepo, J. C., López, J. A., Valmori, D., Corradin, G., & Herrera, S. (2002). Identification of HLA‐A2 restricted CD8+ T‐lymphocyte responses to Plasmodium vivax circumsporozoite protein in individuals naturally exposed to malaria. Parasite Immunology, 24(3), 161-169. https://doi.org/10.1046/j.1365-3024.2002.00449.x

  • Azam, F. M., Zamri-Saad, M., Rahim, R. A., Chumnanpoend, P., E-kobon, T., & Othman, S. (2020). Antigenic outer membrane proteins prediction of Pasteurella multocida serotype B:2. Asia-Pacific Journal of Molecular Biology and Biotechnology, 28(4), 102-116. https://doi.org/10.35118/apjmbb.2020.028.4.09

  • Balch, W. E., Morimoto, R. I., Dillin, A., & Kelly, J. W. (2008). Adapting proteostasis for disease intervention. Science, 319(5865), 916–919. https://doi.org/10.1126/science.1141448

  • Baliga, P., Shekar, M., & Venugopal, M. N. (2018). Potential outer membrane protein candidates for vaccine development against the pathogen Vibrio anguillarum: A reverse vaccinology based identification. Current Microbiology, 75(3), 368-377. https://doi.org/10.1007/s00284-017-1390-z

  • 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

  • Benkert, P., Künzli, M., & Schwede, T. (2009). QMEAN server for protein model quality estimation. Nucleic Acids Research, 37(suppl_2), W510-W514. https://doi.org/10.1093/nar/gkp322

  • Benkirane, A., & De Alwis, M. C. L. (2002). Haemorrhagic septicaemia, its significance, prevention and control in Asia. Veterinary Medicine Journal, 47(8), 234-240. https://doi.org/10.17221/5830-VETMED

  • Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., & Zardecki, C. (2002). The protein data bank. Acta Crystallographica Section D: Biological Crystallography, 58(6), 899-907. https://doi.org/10.1107/S0907444902003451

  • Bhattacharya, M., Sharma, A. R., Sharma, G., Patra, P., Mondal, N., Patra, B. C., Lee, S.-S., & Chakraborty, C. (2020). Computer aided novel antigenic epitopes selection from the outer membrane protein sequences of Aeromonas hydrophila and its analyses. Infection, Genetics and Evolution, 82, 104320. https://doi.org/10.1016/j.meegid.2020.104320

  • Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., & Schwede, T. (2014). SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(W1), W252-W258. https://doi.org/10.1093/nar/gku340

  • Botos, I., Noinaj, N., & Buchanan, S. K. (2017). Insertion of proteins and lipopolysaccharide into the bacterial outer membrane. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1726), 20160224. https://doi.org/10.1098/rstb.2016.0224

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics, 10, 421. https://doi.org/10.1186/1471-2105-10-421

  • Cascales, E., & Lloubès, R. (2004). Deletion analyses of the peptidoglycan‐associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Molecular Microbiology, 51(3), 873-885. https://doi.org/10.1046/j.1365-2958.2003.03881.x

  • Chan, W. C., Liang, P. H., Shih, Y. P., Yang, U. C., Lin, W. C., & Hsu, C. N. (2010). Learning to predict expression efficacy of vectors in recombinant protein production. BMC Bioinformatics, 11(Suppl 1), S21. https://doi.org/10.1186/1471-2105-11-S1-S21

  • Chang, S. T., Ghosh, D., Kirschner, D. E., & Linderman, J. J. (2006). Peptide length-based prediction of peptide–MHC class II binding. Bioinformatics, 22(22), 2761-2767. https://doi.org/10.1093/bioinformatics/btl479

  • Chen, J., Liu, H., Yang, J., & Chou, K. C. (2007). Prediction of linear B-cell epitopes using amino acid pair antigenicity scale. Amino Acids, 33(3), 423-428. https://doi.org/10.1007/s00726-006-0485-9

  • Chin, C. F., Teh, B. A., Anthony, A. A., Aziah, I., Ismail, A., Ong, E. B. B., & Lim, T. S. (2014). Overexpression, purification and validation of antigenic Salmonella enterica serovar Typhi proteins identified from LC-MS/MS. Applied Biochemistry and Biotechnology, 174, 1897-1906. https://doi.org/10.1007/s12010-014-1173-y

  • Chung, S. Y., & Subbiah, S. (1996). A structural explanation for the twilight zone of protein sequence homology. Structure, 4(10), 1123-1127. https://doi.org/10.1016/S0969-2126(96)00119-0

  • Ciryam, P., Tartaglia, G. G., Morimoto, R. I., Dobson, C. M., & Vendruscolo, M. (2013). Neurodegenerative diseases and widespread aggregation are associated with supersaturated proteins. Cell Reports, 5(3), 781-790. https://doi.org/10.1016/j.celrep.2013.09.043 PMID: 24183671

  • Collins, R. F., & Derrick, J. P. (2007). Wza: A new structural paradigm for outer membrane secretory proteins?. Trends in Microbiology, 15(3), 96-100. https://doi.org/10.1016/j.tim.2007.01.002

  • Colovos, C., & Yeates, T. (1993). ERRAT: An empirical atom-based method for validating protein structures. Protein Science, 2(9), 1511-1519. https://doi.org/10.1002/pro.5560020916

  • Dong, C., Beis, K., Nesper, J., Brunkan-LaMontagne, A. L., Clarke, B. R., Whitfield, C., & Naismith, J. H. (2006). Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature, 444(7116), 226-229. https://doi.org/10.1038/nature05267

  • Doytchinova, I. A., & Flower, D. R. (2007). VaxiJen: A server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics, 8, 4. https://doi.org/10.1186/1471-2105-8-4

  • EL-Manzalawy, Y., Dobbs, D., & Honavar, V. (2008a). Predicting linear B‐cell epitopes using string kernels. Journal of Molecular Recognition, 21(4), 243-255. https://doi.org/10.1002/jmr.893

  • EL-Manzalawy, Dobbs, D., & Honavar, V. (2008b). Predicting flexible length linear B-cell epitopes. Computational Systems Bioinformatics, 7, 121-132. https://doi.org/10.1142/9781848162648_0011

  • Fisch, A., Reynisson, B., Benedictus, L., Nicastri, A., Vasoya, D., Morrison, I., Buus, S., Ferreira, B. R., de Miranda Santos, I. K. F., Ternette, N., Connelley, T., & Nielsen, M. (2021). Integral use of immunopeptidomics and immunoinformatics for the characterization of antigen presentation and rational identification of BoLA-DR–presented peptides and epitopes. Journal of Immunology, 206(10), 2489-2497. https://doi.org/10.4049/jimmunol.2001409

  • Fiser, A., & Šali, A. (2003). Modeller: Generation and refinement of homology-based protein structure models. Methods in Enzymology, 374, 461-491. https://doi.org/10.1016/S0076-6879(03)74020-8

  • Ford, R. C., Brunkan-LaMontagne, A. L., Collins, R. F., Clarke, B. R., Harris, R., Naismith, J. H., & Whitfield, C. (2009). Structure–function relationships of the outer membrane translocon Wza investigated by cryo-electron microscopy and mutagenesis. Journal of Structural Biology, 166(2), 172-182. https://doi.org/10.1016/j.jsb.2009.02.005

  • Haddad, Y., Adam, V., & Heger, Z. (2020). Ten quick tips for homology modeling of high- resolution protein 3D structures. PLOS Computational Biology, 16(4), e1007449. https://doi.org/10.1371/JOURNAL.PCBI.1007449

  • Harper, M., Boyce, J. D., & Adler, B. (2006). Pasteurella multocida pathogenesis: 125 years after pasteur. FEMS Microbiology Letters, 265(1), 1–10. https://doi.org/10.1111/j.1574-6968.2006.00442.x

  • Hasan, M. A., Khan, M. A., Datta, A., Mazumder, M. H. H., & Hossain, M. U. (2015). A comprehensive immunoinformatics and target site study revealed the corner-stone toward Chikungunya virus treatment. Molecular Immunology, 65(1), 189-204. https://doi.org/10.1016/j.molimm.2014.12.013

  • Hasani, H. J., & Barakat, K. H. (2016). Protein-protein docking: Are we there yet?. In Methods and algorithms for molecular docking-based drug design and discovery (pp. 173-195). IGI Global. https://doi.org/10.4018/978-1-5225-0115-2.ch007

  • Hatfaludi, T., Al-Hasani, K., Gong, L., Boyce, J. D., Ford, M., Wilkie, I. W., Quinsey, N., Dunstone, M. A. Hoke, D. E., & Adler, B. (2012). Screening of 71 P. multocida proteins for protective efficacy in a fowl cholera infection model and characterization of the protective antigen PlpE. PLOS One, 7(7), e39973. https://doi.org/10.1371/journal.pone.0039973

  • Hensen, U., Meyer, T., Haas, J., Rex, R., Vriend, G., & Grubmüller, H. (2012). Exploring protein dynamics space: The dynasome as the missing link between protein structure and function. PLOS One, 7(5), e33931. https://doi.org/10.1371/journal.pone.0033931

  • Jabeen, S., Yap, H. Y., Abdullah, F. F. J., Zakaria, Z., Isa, N. M., Tan, Y. C., Joo, Y. S., Satharasinghe, D. A., & Omar, A. R. (2019). Complete genome sequence analysis and characterization of selected iron regulation genes of Pasteurella multocida serotype A strain PMTB2.1. Genes, 10(2), 81. https://doi.org/10.3390/genes10020081

  • Jabeen, S., Yong, Y. H., Abdullah, F. J. F., Zakaria, Z., Mat Isa, N., Tan, Y. C., Yee, W. Y., & Omar, A. R. (2017). Complete genome sequence of Pasteurella multocida serotype A strain PMTB2.1 isolated from buffaloes that died of septicemia in Malaysia. Genome Announcements, 5(44), e01190-17. https://doi.org/10.1128/genomeA.01190-17

  • Jenkins, M. K., Khoruts, A., Ingulli, E., Mueller, D. L., McSorley, S. J., Reinhardt, R. L., Itano, A., & Pape, K. A. (2003). In vivo activation of antigen-specific CD4 T cells. Annual Reviews of Immunology, 19, 23–45. https://doi.org/10.1146/annurev.immunol.19.1.23

  • Jiménez-García, B., Roel-Touris, J., Romero-Durana, M., Vidal, M., Jiménez-González, D., & Fernández-Recio, J. (2018). LightDock: A new multi-scale approach to protein–protein docking. Bioinformatics, 34(1), 49–55. https://doi.org/10.1093/bioinformatics/btx555

  • Jones, P. M., & George, A. M. (2004). The ABC transporter structure and mechanism: Perspectives on recent research. Cellular and Molecular Life Sciences, 61(6), 682-699. https://doi.org/10.1007/s00018-003-3336-9

  • Joshi, S., Tewari, K., & Singh, R. (2013). Comparative immunogenicity and protective efficacy of different preparations of outer membrane proteins of Pasteurella multocida (B:2) in a mouse model. Veterinarski Arhiv, 83(6), 665-676.

  • Karami, Y., Rey, J., Postic, G., Murail, S., Tufféry, P., & De Vries, S. J. (2019). DaReUS- Loop: A web server to model multiple loops in homology models. Nucleic Acids Research, 47(W1), W423-W428. https://doi.org/10.1093/nar/gkz403

  • Kim, M., Song, L., Moon, J., Sun, Z. Y., Bershteyn, A., Hanson, M., Cain, D., Goka, S., Kelsoe, G., Wagner, G., Irvine, D., & Reinherz, E. L. (2013). Immunogenicity of membrane-bound HIV-1 gp41 membrane-proximal external region (MPER) segments is dominated by residue accessibility and modulated by stereochemistry. Journal of Biological Chemistry, 288(44), 31888–31901. https://doi.org/10.1074/jbc.M113.494609

  • Kong, L., Harrington, L., Li, Q., Cheley, S., Davis, B. G., & Bayley, H. (2013). Single-molecule interrogation of a bacterial sugar transporter allows the discovery of an extracellular inhibitor. Nature Chemistry, 5(8), 651–659. https://doi.org/10.1038/nchem.1695

  • Kumar, A., Mohanty, N. N., Chacko, N., Yogisharadhya, R., & Shivachandra, S. B. (2015). Structural features of a highly conserved Omp16 protein of Pasteurella multocida strains and comparison with related peptidoglycan-associated lipoproteins (PAL). Indian Journal of Microbiology, 55(1), 50-56. https://doi.org/10.1007/s12088-014-0489-1

  • 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

  • Lazzaroni, J. C., & Portalier, R. (1992). The excC gene of Escherichia coli K‐12 required for cell envelope integrity encodes the peptidoglycan‐associated lipoprotein (PAL). Molecular Microbiology, 6(6), 735-742. https://doi.org/10.1111/j.1365-2958.1992.tb01523.x

  • Liu, N., & Xu, Z. (2019). Using LeDock as a docking tool for computational drug design. In IOP Conference Series: Earth and Environmental Science (Vol. 218, No. 1, p. 012143). IOP Publishing. https://doi.org/10.1088/1755-1315/218/1/012143

  • Liu, W., Yang, M., Xu, Z., Zheng, H., Liang, W., Zhou, R., Wu, B., & Chen, H. (2012). Complete genome sequence of Pasteurella multocida HN06, a toxigenic strain of serogroup D. Journal of Bacteriology, 194(12), 3292-3293. https://doi.org/10.1128/JB.00215-12

  • Magnan, C. N., Zeller, M., Kayala, M. A., Vigil, A., Randall, A., Felgner, P. L., & Baldi, P. (2010). High-throughput prediction of protein antigenicity using protein microarray data. Bioinformatics, 26(23), 2936-2943. https://doi.org/10.1093/bioinformatics/btq551

  • Martz, F. (2014). Développement d’une nouvelle méthode de docking basée sur les mécanismes enzymatiques et guidée par des groupes prosthétiques [Development of a new mechanism-based molecular docking method guided by prosthetic groups] [Doctoral dissertation, Université Paris Sud-Paris XI]. HAL Portal Theses. https://tel.archives-ouvertes.fr/tel-01168482

  • Mathelié-Guinlet, M., Asmar, A. T., Collet, J. F., & Dufrêne, Y. F. (2020). Bacterial cell mechanics beyond peptidoglycan. Trends in Microbiology, 28(9), 706-708. https://doi.org/10.1016/j.tim.2020.04.013

  • May, B. J., Zhang, Q., Li, L. L., Paustian, M. L., Whittam, T. S., & Kapur, V. (2001). Complete genomic sequence of Pasteurella multocida, Pm70. Proceedings of the National Academy of Sciences, 98(6), 3460-3465. https://doi.org/10.1073/pnas.051634598

  • Muenthaisong, A., Nambooppha, B., Rittipornlertrak, A., Tankaew, P., Varinrak, T., Muangthai, K., Atthikanyaphak, K., Sawada, T., & Sthitmatee, N. (2020). An intranasal vaccination with a recombinant outer membrane protein H against haemorrhagic septicemia in swamp buffaloes. Veterinary Medicine International, 2020, 3548973. https://doi.org/10.1155/2020/3548973

  • Naz, A., Awan, F. M., Obaid, A., Muhammad, S. A., Paracha, R. Z., Ahmad, J., & Ali, A. (2015). Identification of putative vaccine candidates against Helicobacter pylori exploiting exoproteome and secretome: A reverse vaccinology based approach. Infection, Genetics and Evolution, 32, 280-291. https://doi.org/10.1016/j.meegid.2015.03.027

  • Park, H., Lee, G. R., Heo, L., & Seok, C. (2014). Protein loop modeling using a new hybrid energy function and its application to modeling in inaccurate structural environments. PLOS One, 9(11), e113811. https://doi.org/10.1371/journal.pone.0113811

  • Patronov, A., & Doytchinova, I. (2013). T-cell epitope vaccine design by immunoinformatics. Open Biology, 3(1), 120139. https://doi.org/10.1098/rsob.120139

  • Peng, Z., Liang, W., Liu, W., Wu, B., Tang, B., Tan, C., Zhou, R., & Chen, H. (2016). Genomic characterization of Pasteurella multocida HB01, a serotype A bovine isolate from China. Gene, 581(1), 85-93. https://doi.org/10.1016/j.gene.2016.01.041

  • Peng, Z., Liang, W., Wang, F., Xu, Z., Xie, Z., Lian, Z., Hua, L., Zhou, Z., Chen, H., & Wu, B. (2018). Genetic and phylogenetic characteristics of Pasteurella multocida isolates from different host species. Frontiers in Microbiology, 9, 1408. https://doi.org/10.3389/fmicb.2018.01408

  • Peng, Z., Wang, X., Zhou, R., Chen, H., Wilson, B. A., & Wu, B. (2019). Pasteurella multocida: Genotypes and genomics. Microbiology and Molecular Biology Reviews, 83(4), e00014-19. https://doi.org/10.1128/MMBR.00014-19

  • Prajapat, R., Marwal, A., & Gaur, R. K. (2014). Recognition of errors in the refinement and validation of three-dimensional structures of AC1 proteins of Begomovirus strains by using ProSA-web. Journal of Viruses, 2014, 752656. https://doi.org/10.1155/2014/752656

  • Prasannavadhana, A., Kumar, S., Thomas, P., Sarangi, L. N., Gupta, S. K., Priyadarshini, A., Nagaleekar, V. K., & Singh, V. P. (2014). Outer membrane proteome analysis of Indian strain of Pasteurella multocida serotype B:2 by MALDI-TOF/MS analysis. The Scientific World Journal, 2014, 617034. https://doi.org/10.1155/2014/617034

  • Qiao, S., Luo, Q., Zhao, Y., Zhang, X. C., & Huang, Y. (2014). Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature, 511(7507), 108-111. https://doi.org/10.1038/nature13484

  • Rafidah, O., Zamri-Saad, M., Nasip, E., Shahiruddin, S., & Saharee, A. A. (2010). Analysis of haemorrhagic septicaemia outbreaks in cattle and buffalo in Malaysia. Online Journal of Veterinary Research, 14(2), 325-333.

  • Rahman, M. S., Biswas, C., Biswas, P. K., Kader, M. A., Alam, S. N., Sonne, C., & Kim, K. H. (2020). In silico analysis of the antigenic properties of iron-regulated proteins against Neisseria meningitidis. Applied Sciences, 10(17), 6113. https://doi.org/10.3390/app10176113

  • Ramachandran, G. N., Ramakrishnan, C., & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology, 7(1), 95–99. https://doi.org/10.1016/S0022-2836(63)80023-6

  • Reid, A. N., & Whitfield, C. (2005). Functional analysis of conserved gene products involved in assembly of Escherichia coli capsules and exopolysaccharides: Evidence for molecular recognition between Wza and Wzc for colanic acid biosynthesis. Journal of Bacteriology, 187(15), 5470-5481. https://doi.org/10.1128/JB.187.15.5470-5481.2005

  • Remmert, M., Biegert, A., Hauser, A., & Söding, J. (2012). HHblits: Lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nature Methods, 9, 173-175. https://doi.org/10.1038/nmeth.1818

  • Rimler, R. B. (2001). Purification of a cross-protective antigen from Pasteurella multocida grown in vitro and in vivo. Avian Diseases, 45(3), 572-580. https://doi.org/10.2307/1592897

  • Rita, D. V., Swee, K. C. W., Shamini, C., Kang, T. L., Nurshamimi, N. R., Hussin, A. R., Nurul, K., & Salmah, I. (2018). A recombinant subunit HSABA392 as a potential vaccine for haemorrhagic septicaemia disease in livestock. Tropical Biomedicine, 35(4), 1075-1086.

  • Sailapathi, A., Murugan, G., Somarathinam, K., Gunalan, S., Jagadeesan, R., Yoosuf, N., Kanagaraj, S., & Kothandan, G. (2020). Proposing the promiscuous protein structures in JNK1 and JNK3 for virtual screening in pursuit of potential leads. ACS Omega, 5(8), 3969–3978. https://doi.org/10.1021/acsomega.9b03458

  • Sarah, S. O., Zamri-Saad, M., Zunita, Z., & Raha, A. R. (2006). Molecular cloning and sequence analysis of gdhA gene of Pasteurella multocida B:2. Journal of Animal and Veterinary Advances, 5(12), 1146- 1149.

  • Shen, W., Cao, Y., Cha, L., Zhang, X., Ying, X., Zhang, W., Ge, K., Li, W., & Zhong, L. (2015). Predicting linear B-cell epitopes using amino acid anchoring pair composition. BioData Mining, 8, 14. https://doi.org/10.1186/s13040-015-0047-3

  • Sippel, K. H., Robbins, A. H., Reutzel, R., Boehlein, S. K., Namiki, K., Goodison, S., Agbandje, M. M., Rosser, C. J., & McKenna, R. (2009). Structural insights into the extracytoplasmic thiamine-binding lipoprotein p37 of Mycoplasma hyorhinis. Journal of Bacteriology, 191(8), 2585-2592. https://doi.org/10.1128/JB.01680-08

  • Sollner, J., Grohmann, R., Rapberger, R., Perco, P., Lukas, A., & Mayer, B. (2008). Analysis and prediction of protective continuous B-cell epitopes on pathogen proteins. Immunome Research, 4, 1. https://doi.org/10.1186/1745-7580-4-1

  • Soriano, E. V., Rajashankar, K. R., Hanes, J. W., Bale, S., Begley, T. P., & Ealick, S. E. (2008). Structural similarities between thiamin-binding protein and thiaminase-I suggest a common ancestor. Biochemistry, 47(5), 1346-1357. https://doi.org/10.1021/bi7018282

  • Trolle, T., McMurtrey, C. P., Sidney, J., Bardet, W., Osborn, S. C., Kaever, T., Sette, A., Hildebrand, W. H., Nielsen, M., & Peters, B. (2016). The length distribution of class I–restricted T cell epitopes is determined by both peptide supply and MHC allele–specific binding preference. The Journal of Immunology, 196(4), 1480-1487. https://doi.org/10.4049/jimmunol.1501721

  • Villa, R., Martorana, A. M., Okuda, S., Gourlay, L. J., Nardini, M., Sperandeo, P., Dehò, G., Bolognesi, M., Kahne, D., & Polissi, A. (2013). The Escherichia coli Lpt transenvelope protein complex for lipopolysaccharide export is assembled via conserved structurally homologous domains. Journal of Bacteriology, 195(5), 1100-1108. https://doi.org/10.1128/JB.02057-12

  • Wang, J., & Dokholyan, N. V. (2019). MedusaDock 2.0: Efficient and accurate protein–ligand docking with constraints. Journal of Chemical Information and Modeling, 59(6), 2509–2515. https://doi.org/10.1021/acs.jcim.8b00905

  • 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

  • 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(suppl_2), W407-W410. https://doi.org/10.1093/nar/gkm290

  • Zamri-Saad, M., & Annas, S. (2016). Vaccination against hemorrhagic septicemia of bovines: A review. Pakistan Veterinary Journal, 36(1), 1-5.

ISSN 1511-3701

e-ISSN 2231-8542

Article ID

JTAS-2540-2022

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