Protective effects of Staphylococcal Enterotoxin B (SEB) toxoid on lung and liver tissue integrity in rats during systemic infection
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Abstract
Background and Objectives: Staphylococcal enterotoxin B (SEB), a potent superantigenic toxin produced by Staphylococcus aureus (S. aureus), plays a crucial role in S. aureus systemic infection. This investigation sought to determine whether immunising animals with SEB toxoid could protect against an experimental acute systemic infection caused by S. aureus.
Materials and Methods: This study involved three groups of animals: one group was administered with SEB toxoid, and the second group was administered with intramuscular injections of normal saline, after which both were subjected to systemic S. aureus infection. The third group served as the negative control. After two weeks, the outcomes of the experimental systemic infection demonstrated that SEB immunisation significantly shielded organs (lung and liver) from damage in comparison to the control group.
Results: Regarding the histopathological analysis of liver and lung tissues, the control group showed minimal alterations, indicating a normal tissue state. Infected individuals exhibited severe pathology, including inflammation, necrosis, and fibrosis. The immunised group displayed a mixed profile with elevated inflammation but lower necrosis and fibrosis. Immunisation mitigated pathological changes induced by infection, fostering a more controlled response.
Conclusion: SEB plays an important role in S. aureus pathogenesis and immunisation, and this toxoid might protect against fatal infections of S. aureus.
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16. Kim SW, Roh J, Park CS. Immunohistochemistry for Pathologists: Protocols, Pitfalls, and Tips. J Pathol Transl Med 2016; 50: 411-418.
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18. Alsultan A, Alsallami D. Efflux-mediated bile resistance in Gram-positive pathogens. J Pure Appl Microbiol 2022; 16: 10-17.
19. Chmiel JF, Aksamit TR, Chotirmall SH, Dasenbrook EC, Elborn JS, LiPuma JJ, et al. Antibiotic management of lung infections in cystic fibrosis. I. The microbiome, methicillin-resistant Staphylococcus aureus, gram-negative bacteria, and multiple infections. Ann Am Thorac Soc 2014; 11: 1120-1129.
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22. Morimoto C, Matsumoto H, Ito I, Nagaski T, Oguma T, Hirai T. Roles of Staphylococcus aureus and sensitization to staphylococcal enterotoxin in bronchiectasis. Respir Investig 2023; 61: 23-26.
23. Alsultan A, Al-Sallami D, Alsaadi M. Antibiotic resistance genes in farm animal slaughterhouse wastes in Al-Dewanyiah province, Iraq. Vet Integr Sci 2023; 21: 577-586.
24. Sause WE, Buckley PT, Strohl WR, Lynch AS, Torres VJ. Antibody-based biologics and their promise to combat Staphylococcus aureus infections. Trends Pharmacol Sci 2016; 37: 231-241.
25. Rajagopalan G, Sen MM, Singh M, Murali NS, Nath KA, Iijima K, et al. Intranasal exposure to staphylococcal enterotoxin B elicits an acute systemic inflammatory response. Shock 2006; 25: 647-656.
26. Jang JH, Kim S, Kim SG, Lee J, Lee DG, Jang J, et al. A sensitive immunodetection assay using antibodies specific to staphylococcal enterotoxin B produced by baculovirus expression. Biosensors (Basel) 2022; 12: 787.
27. Rahman S, Sarkar K, Das AK. Exploring staphylococcal superantigens to design a potential multi-epitope vaccine against Staphylococcus aureus: an in-silico reverse vaccinology approach. J Biomol Struct Dyn 2023; 41: 13098-13112.
28. Wan Q, Zhou J, Wu Y, Shi L, Liu W, Ou J, et al. TNF-α-mediated podocyte injury via the apoptotic death receptor pathway in a mouse model of IgA nephropathy. Ren Fail 2022; 44: 1216-1226.
29. Mohammad H, Abutaleb NS, Dieterly AM, Lyle LT, Seleem MN. Evaluation of ebselen in resolving a methicillin-resistant Staphylococcus aureus infection of pressure ulcers in obese and diabetic mice. PLoS One 2021; 16(2): e0247508.
2. Bae JS, Da F, Liu R, He L, Lv H, Fisher EL, et al. Contribution of staphylococcal enterotoxin B to Staphylococcus aureus systemic infection. J Infect Dis 2021; 223: 1766-1775.
3. Cavaiuolo M, Lefebvre D, Mutel I, Vingadassalon N, Merda D, Hennekinne J-A, et al. First report of enterotoxigenic Staphylococcus argenteus as a foodborne pathogen. Int J Food Microbiol 2023; 394: 110182.
4. Purwanasari HN, Permatasari ATU, Lestari FB, Wasissa M, Zaini K, Salasia SIO. Cellular immune response of Staphylococcus aureus enterotoxin B in Balb/c mice through intranasal infection. Vet World 2022; 15: 1765-1771.
5. Al-Sallami D, Alsultan A, Abbas KH, Clarke SR. Evaluation of efflux pump inhibitory activity of some plant extracts and using them as adjuvants to potentiate the inhibitory activity of some antibiotics against Staphylococcus aureus. Open Vet J 2023; 13: 42-47.
6. Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003; 41: 1434-1439.
7. Choi JY, Shin S, Kim NY, Son WS, Kang TJ, Song DH, et al. A novel staphylococcal enterotoxin B subunit vaccine candidate elicits protective immune response in a mouse model. Toxicon 2017; 131: 68-77.
8. Piszczek P, Wójcik-Piotrowicz K, Nowak B, Guzdek P, Novak P, Pytko-Polonczyk J, et al. Phagocytosis of latex beads by a human monocytic Mono Mac 6 cell line and effects of low-frequency electromagnetic field interaction. J Physiol Pharmacol 2023; 74: 10.26402/jpp.2023.2.10.
9. Xiaodong X, Tao L, Jianmin L, Jing Z, Bing Z, Jintao D, et al. Crocin Inhibits the Type 2 Inflammatory Response Produced by ILC2s in Eosinophilic Nasal Polyps. Am J Rhinol Allergy 2023; 37: 656-669.
10. Berry SC, Triplett OA, Yu L-R, Hart ME, Jackson LS, Tolleson WH. Microcalorimetric Investigations of reversible Staphylococcal enterotoxin Unfolding. Toxins (Basel) 2022; 14: 554.
11. DeLorenzo DM, Moon TS. Selection of stable reference genes for RT-qPCR in Rhodococcus opacus PD630. Sci Rep 2018; 8: 6019.
12. Clegg J, Soldaini E, McLoughlin RM, Rittenhouse S, Bagnoli F, Phogat S. Staphylococcus aureus Vaccine research and Development: the past, Present and future, including novel Therapeutic Strategies. Front Immunol 2021; 12: 705360.
13. Banaszkiewicz S, Tabiś A, Wałecki B, Łyżwińska K, Bystroń J, Bania J. Spa types and Staphylococcal Enterotoxin production of Staphylococcus aureus isolated from Wild Boar. Microb Ecol 2023; 86: 2184-2191.
14. Zhao Z, Sun H-Q, Wei S-S, Li B, Feng Q, Zhu J, et al. Multiple B-cell epitope vaccine induces a Staphylococcus enterotoxin B-specific IgG1 protective response against MRSA infection. Sci Rep 2015; 5: 12371.
15. Kashiwada T, Kikuchi K, Abe S, Kato H, Hayashi H, Morimoto T, et al. Staphylococcal enterotoxin B toxic shock syndrome induced by community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA). Intern Med 2012; 51: 3085-3088.
16. Kim SW, Roh J, Park CS. Immunohistochemistry for Pathologists: Protocols, Pitfalls, and Tips. J Pathol Transl Med 2016; 50: 411-418.
17. Ahmad-Mansour N, Loubet P, Pouget C, Dunyah-Remy C, Sotto A, Lavigne J-P, et al. Staphlococcus aureus Toxins: An update on their pathogenic Propertiesand Potential Treatments. Toxins (Basel) 2021; 13: 677.
18. Alsultan A, Alsallami D. Efflux-mediated bile resistance in Gram-positive pathogens. J Pure Appl Microbiol 2022; 16: 10-17.
19. Chmiel JF, Aksamit TR, Chotirmall SH, Dasenbrook EC, Elborn JS, LiPuma JJ, et al. Antibiotic management of lung infections in cystic fibrosis. I. The microbiome, methicillin-resistant Staphylococcus aureus, gram-negative bacteria, and multiple infections. Ann Am Thorac Soc 2014; 11: 1120-1129.
20. Gholipour Z, Fooladi AAI, Parivar K, Halabian R. Targeting glioblastoma multiforme using a novel fusion protein comprising interleukin-13 and staphylococcal enterotoxin B in vitro. Toxicol In Vitro 2023; 92: 105651.
21. Hu D-L, Nakane A. Mechanisms of staphylococcal enterotoxin-induced emesis. Eur J Pharmacol 2014; 722: 95-107.
22. Morimoto C, Matsumoto H, Ito I, Nagaski T, Oguma T, Hirai T. Roles of Staphylococcus aureus and sensitization to staphylococcal enterotoxin in bronchiectasis. Respir Investig 2023; 61: 23-26.
23. Alsultan A, Al-Sallami D, Alsaadi M. Antibiotic resistance genes in farm animal slaughterhouse wastes in Al-Dewanyiah province, Iraq. Vet Integr Sci 2023; 21: 577-586.
24. Sause WE, Buckley PT, Strohl WR, Lynch AS, Torres VJ. Antibody-based biologics and their promise to combat Staphylococcus aureus infections. Trends Pharmacol Sci 2016; 37: 231-241.
25. Rajagopalan G, Sen MM, Singh M, Murali NS, Nath KA, Iijima K, et al. Intranasal exposure to staphylococcal enterotoxin B elicits an acute systemic inflammatory response. Shock 2006; 25: 647-656.
26. Jang JH, Kim S, Kim SG, Lee J, Lee DG, Jang J, et al. A sensitive immunodetection assay using antibodies specific to staphylococcal enterotoxin B produced by baculovirus expression. Biosensors (Basel) 2022; 12: 787.
27. Rahman S, Sarkar K, Das AK. Exploring staphylococcal superantigens to design a potential multi-epitope vaccine against Staphylococcus aureus: an in-silico reverse vaccinology approach. J Biomol Struct Dyn 2023; 41: 13098-13112.
28. Wan Q, Zhou J, Wu Y, Shi L, Liu W, Ou J, et al. TNF-α-mediated podocyte injury via the apoptotic death receptor pathway in a mouse model of IgA nephropathy. Ren Fail 2022; 44: 1216-1226.
29. Mohammad H, Abutaleb NS, Dieterly AM, Lyle LT, Seleem MN. Evaluation of ebselen in resolving a methicillin-resistant Staphylococcus aureus infection of pressure ulcers in obese and diabetic mice. PLoS One 2021; 16(2): e0247508.
| Files | ||
| Issue | Vol 17 No 2 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i2.18396 | |
| Keywords | ||
| SEB; Methicillin-resistant Staphylococcus aureus; Pathogenesis; Immunization; Tissue damage; Experimental infection | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Rasheed Al-Fetly D, Ghanim Rhyaf A, Abbas Naji H. Protective effects of Staphylococcal Enterotoxin B (SEB) toxoid on lung and liver tissue integrity in rats during systemic infection. Iran J Microbiol. 2025;17(2):220-228.
