Immunogenicity Evaluation of Recombinant Staphylococcus aureus Enterotoxin B (rSEB) and rSEB-loaded Chitosan Nanoparticles Following Nasal Administration
,
Abstract
Staphylococcal enterotoxin B (SEB), apotent superantigen, is responsible for many disorders caused by Staphylococcus aureus. With regard to the appearance of multidrug-resistant strains of the bacteria, there is a great need to develop an efficient vaccine against this pathogen. In the present study, the immunogenicity of recombinant SEB was evaluated following nasal administration to BABLB/c mice. Indeed, the rSEB protein was entrapped into chitosan nanoparticles and the immunogenicity of nano-formulation was investigated. SEB protein was expressed in E. coli BL21 (DE3) and purified by using a nickel column. Chitosan nanoparticles were synthesized in the presence of rSEB; using the ionic gelation technique. Synthesized NPs containing rSEB and bare rSEB were administered to mice nasally. Serum and stool IgG and IgA antibody showed that both formulations were able to evoke the mice's immune responses and there was no significant difference between them. Results of the toxin neutralization test on Vero cells indicated that the sera of the immunized mice had an inhibitory effect on the growth of these cells (p<0.001). Nasal administration of bare rSEB could efficiently simulate the mice's immune system and nano-delivery of this protein via nasal route had not a significant impact on its immunogenicity improvement.
1. Wakabayashi Y, Umeda K, et al. Staphylococcal food poisoning caused by Staphylococcus argenteus harboring staphylococcal enterotoxin genes. Int. J. Food Microbiol. 2018;265:23-9.
2. Rahimi F, Bouzari M, Katoli M, Pourshafi M. The prevalence Methicillin-resistant Staphylococcus aureus strains produce enterotoxin A in Tehran hospitals. Iran J Infect Dis Trop Med. 2014;19(65):59-68.
3. Murray R. Recognition and management of Staphylococcus aureus toxin‐mediated disease. Intern. Med. J. 2005;35:S106-S19.
4. Thomas D, Chou S, Dauwalder O, Lina G. Diversity in Staphylococcus aureus enterotoxins. Superantigens and Superallergens. 93: Karger Publishers; 2007. p. 24-41.
5. Norouzi J, Goudarzi G, Pakzad P, Razavipour R. The isolation and detection of Staphylococcus aureus enterotoxins AE and TSST-1 genes from different sources by PCR method. Qom Univ. Med. Sci. J. 2012;6(3):78-85.
6. Hassoun A, Linden PK, Friedman B. Incidence, prevalence, and management of MRSA bacteremia across patient populations—a review of recent developments in MRSA management and treatment. Crit. Care Med.. 2017;21(1):211.
7. Ansari S, Jha RK, Mishra SK, Tiwari BR, Asaad AM. Recent advances in Staphylococcus aureus infection: focus on vaccine development. Infect. Drug Resist. 2019;12:1243.
8. Redi D, Raffaelli CS, Rossetti B, et al. Staphylococcus aureus vaccine preclinical and clinical development: current state of the art. New Microbiol. 2018;41:208-13.
9. LeClaire RD, Hunt RE, Bavari S. Protection against bacterial superantigen staphylococcal enterotoxin B by passive vaccination. Infect. Immun.. 2002;70(5):2278-81.
10. Michie CA. Staphylococcal vaccines. Trends Immunol. 2002;23(9):461-3.
11. Hale ML. Staphylococcal Enterotoxins, Staphylococcal Enterotoxin B and Bioterrorism. Bioterrorism: IntechOpen. 2012.
12. Karauzum H, Chen G, Abaandou L, Mahmoudieh M, Boroun AR, Shulenin S, et al. Synthetic human monoclonal antibodies toward staphylococcal enterotoxin B (SEB) protective against toxic shock syndrome.J. Biol. Chem. 2012;287(30):25203-15.
13. Coffman JD, Zhu J, Roach JM, Bavari S, Ulrich RG, Giardina SL. Production and purification of a recombinant staphylococcal enterotoxin B vaccine candidate expressed in Escherichia coli. Protein Expression Purif.. 2002;24(2):302-12.
14. Hudson LC, Seabolt BS, Odle J, Bost KL, Stahl CH, Piller KJ. Sublethal staphylococcal enterotoxin B challenge model in pigs to evaluate protection following immunization with a soybean-derived vaccine. Clin. Vaccine Immunol.. 2013;20(1):24-32.
15. Hajizade A, Salmanian AH, Amani J, Ebrahimi F, Arpanaei A. EspA-loaded mesoporous silica nanoparticles can efficiently protect animal model against enterohaemorrhagic E. coli O157: H7. Artif. Cells, Nanomed., Biotechnol. 2018:1-9.
16. Kordbacheh E, Nazarian S, Hajizadeh A, Sadeghi D. Entrapment of LTB protein in alginate nanoparticles protects against Enterotoxigenic Escherichia coli. Apmis. 2018;126(4):320-8.
17. Kordbacheh E, Nazarian S, Sadeghi D, Hajizadeh A. An LTB-entrapped protein in PLGA nanoparticles preserves against nterotoxin of enterotoxigenic Escherichia coli. Iran. J. Basic Med. Sci. 2018;21(5):517.
18. Gause KT, Wheatley AK, Cui J, Yan Y, Kent SJ, Caruso F. Immunological principles guiding the rational design of particles for vaccine delivery. ACS nano. 2017;11(1):54-68.
19. Zhao L, Seth A, Wibowo N, Zhao C-X, Mitter N, Yu C, et al. Nanoparticle vaccines. Vaccine. 2014;32(3):327-37.
20. Mengelizadeh N, Haghighifard NJ, Takdastan A, Hormozinejad M. Physicochemical Characterization of Biopolymer Chitosan Extracted from Shrimp Shells. Sci. Technol.. 2015;27(6):371-80.
21. Kumar A, Vimal A, Kumar A. Why Chitosan? From properties to perspective of mucosal drug delivery. Int. J. Biol. Macromol. 2016;91:615-22.
22. Hosseini SA, Ebrahimi F, Nazarian Sh, Hamidi M. Recombinant Expression of Staphylococcus Aureus Enterotoxin Type B as a Vaccine Candidate. Jundishapur Sci Med J. 2017; 16(6):653-664.
23. Bagheripour MJ, Ebrahimi F, Hajizade A, Nazarian S. Immunogenicity evaluation of rBoNT/E nanovaccine after mucosal administration. Iran. J. Basic Med. Sci.2019;22(4):353.
24. Marques MR, Loebenberg R, Almukainzi M. Simulated biological fluids with possible application in dissolution testing.Dissolution Technol. 2011;18(3):15-28.
25. Ramakrishnan MA. Determination of 50% endpoint titer using a simple formula. J. Virol. 2016;5(2):85.
26. Hayon T, Dvilansky A, Shpilberg O, Nathan I. Appraisal of the MTT-based assay as a useful tool for predicting drug chemosensitivity in leukemia. Leuk. Lymphoma 2003;44(11):1957-62.
27. Hajizade A, Ebrahimi F, Salmanian A-H, Arpanae A, Amani J. Nanoparticles in vaccine development. J. Appl. Biotechnol. Rep. 2015;1(4):pp. 125-34.
28. Fini A, Orienti I. The role of chitosan in drug delivery. Am. J. Drug Delivery 2003;1(1):43-59.
29. Bagheripour M, Ebrahimi F, Hajizadeh A, Nazarian S. Immunogenicity Effect of Chitosan Nanoparticles Containing Botulinum Neurotoxin E binding Domain Recombinant Protein in Mice. J. Mazandaran Univ. Med. Sci. 2015;25(124):37-47.
30. Buelow R, O'Hehir R, Schreifels R, Kummerehl T, Riley G, Lamb J. Localization of the immunologic activity in the superantigen Staphylococcal enterotoxin B using truncated recombinant fusion proteins. J. Immunol. 1992;148(1):1-6.
31. Shang L, Nienhaus K, Nienhaus GU. Engineered nanoparticles interacting with cells: size matters. J. Nanobiotechnol. 2014;12(1):5.
32. Stiles BG, Garza AR, Ulrich RG, Boles JW. Mucosal vaccination with recombinantly attenuated staphylococcal enterotoxin B and protection in a murine model. Infect. Immun. 2001;69(4):2031-6.
33. Bagheripour M, Ebrahimi F, Hajizadeh A, Nazarian S, Arefpour M. Preparation of chitosan-based botulinum neurotoxin e recombinant nanovaccine and evaluation of its immunogenicity as oral & intradermal route in mice. J RafsanjanUniv Med Sci 2016;14(11):923-38.
34. Fernández-Urrusuno R, Calvo P, Remuñán-López C, Vila-Jato JL, Alonso MJ. Enhancement of nasal absorption of insulin using chitosan nanoparticles. Pharm. Res. 1999;16(10):1576-81.
35. Amini Y, Tebianian M, Mosavari N, Fasihi Ramandi M, Ebrahimi S, Dabaghian M, et al. Preparation of ESAT-6 Nanoparticles and Evaluation of Humoral Immunity after Intranasal Administration. JSSU. 2013;20(5):612-26.
2. Rahimi F, Bouzari M, Katoli M, Pourshafi M. The prevalence Methicillin-resistant Staphylococcus aureus strains produce enterotoxin A in Tehran hospitals. Iran J Infect Dis Trop Med. 2014;19(65):59-68.
3. Murray R. Recognition and management of Staphylococcus aureus toxin‐mediated disease. Intern. Med. J. 2005;35:S106-S19.
4. Thomas D, Chou S, Dauwalder O, Lina G. Diversity in Staphylococcus aureus enterotoxins. Superantigens and Superallergens. 93: Karger Publishers; 2007. p. 24-41.
5. Norouzi J, Goudarzi G, Pakzad P, Razavipour R. The isolation and detection of Staphylococcus aureus enterotoxins AE and TSST-1 genes from different sources by PCR method. Qom Univ. Med. Sci. J. 2012;6(3):78-85.
6. Hassoun A, Linden PK, Friedman B. Incidence, prevalence, and management of MRSA bacteremia across patient populations—a review of recent developments in MRSA management and treatment. Crit. Care Med.. 2017;21(1):211.
7. Ansari S, Jha RK, Mishra SK, Tiwari BR, Asaad AM. Recent advances in Staphylococcus aureus infection: focus on vaccine development. Infect. Drug Resist. 2019;12:1243.
8. Redi D, Raffaelli CS, Rossetti B, et al. Staphylococcus aureus vaccine preclinical and clinical development: current state of the art. New Microbiol. 2018;41:208-13.
9. LeClaire RD, Hunt RE, Bavari S. Protection against bacterial superantigen staphylococcal enterotoxin B by passive vaccination. Infect. Immun.. 2002;70(5):2278-81.
10. Michie CA. Staphylococcal vaccines. Trends Immunol. 2002;23(9):461-3.
11. Hale ML. Staphylococcal Enterotoxins, Staphylococcal Enterotoxin B and Bioterrorism. Bioterrorism: IntechOpen. 2012.
12. Karauzum H, Chen G, Abaandou L, Mahmoudieh M, Boroun AR, Shulenin S, et al. Synthetic human monoclonal antibodies toward staphylococcal enterotoxin B (SEB) protective against toxic shock syndrome.J. Biol. Chem. 2012;287(30):25203-15.
13. Coffman JD, Zhu J, Roach JM, Bavari S, Ulrich RG, Giardina SL. Production and purification of a recombinant staphylococcal enterotoxin B vaccine candidate expressed in Escherichia coli. Protein Expression Purif.. 2002;24(2):302-12.
14. Hudson LC, Seabolt BS, Odle J, Bost KL, Stahl CH, Piller KJ. Sublethal staphylococcal enterotoxin B challenge model in pigs to evaluate protection following immunization with a soybean-derived vaccine. Clin. Vaccine Immunol.. 2013;20(1):24-32.
15. Hajizade A, Salmanian AH, Amani J, Ebrahimi F, Arpanaei A. EspA-loaded mesoporous silica nanoparticles can efficiently protect animal model against enterohaemorrhagic E. coli O157: H7. Artif. Cells, Nanomed., Biotechnol. 2018:1-9.
16. Kordbacheh E, Nazarian S, Hajizadeh A, Sadeghi D. Entrapment of LTB protein in alginate nanoparticles protects against Enterotoxigenic Escherichia coli. Apmis. 2018;126(4):320-8.
17. Kordbacheh E, Nazarian S, Sadeghi D, Hajizadeh A. An LTB-entrapped protein in PLGA nanoparticles preserves against nterotoxin of enterotoxigenic Escherichia coli. Iran. J. Basic Med. Sci. 2018;21(5):517.
18. Gause KT, Wheatley AK, Cui J, Yan Y, Kent SJ, Caruso F. Immunological principles guiding the rational design of particles for vaccine delivery. ACS nano. 2017;11(1):54-68.
19. Zhao L, Seth A, Wibowo N, Zhao C-X, Mitter N, Yu C, et al. Nanoparticle vaccines. Vaccine. 2014;32(3):327-37.
20. Mengelizadeh N, Haghighifard NJ, Takdastan A, Hormozinejad M. Physicochemical Characterization of Biopolymer Chitosan Extracted from Shrimp Shells. Sci. Technol.. 2015;27(6):371-80.
21. Kumar A, Vimal A, Kumar A. Why Chitosan? From properties to perspective of mucosal drug delivery. Int. J. Biol. Macromol. 2016;91:615-22.
22. Hosseini SA, Ebrahimi F, Nazarian Sh, Hamidi M. Recombinant Expression of Staphylococcus Aureus Enterotoxin Type B as a Vaccine Candidate. Jundishapur Sci Med J. 2017; 16(6):653-664.
23. Bagheripour MJ, Ebrahimi F, Hajizade A, Nazarian S. Immunogenicity evaluation of rBoNT/E nanovaccine after mucosal administration. Iran. J. Basic Med. Sci.2019;22(4):353.
24. Marques MR, Loebenberg R, Almukainzi M. Simulated biological fluids with possible application in dissolution testing.Dissolution Technol. 2011;18(3):15-28.
25. Ramakrishnan MA. Determination of 50% endpoint titer using a simple formula. J. Virol. 2016;5(2):85.
26. Hayon T, Dvilansky A, Shpilberg O, Nathan I. Appraisal of the MTT-based assay as a useful tool for predicting drug chemosensitivity in leukemia. Leuk. Lymphoma 2003;44(11):1957-62.
27. Hajizade A, Ebrahimi F, Salmanian A-H, Arpanae A, Amani J. Nanoparticles in vaccine development. J. Appl. Biotechnol. Rep. 2015;1(4):pp. 125-34.
28. Fini A, Orienti I. The role of chitosan in drug delivery. Am. J. Drug Delivery 2003;1(1):43-59.
29. Bagheripour M, Ebrahimi F, Hajizadeh A, Nazarian S. Immunogenicity Effect of Chitosan Nanoparticles Containing Botulinum Neurotoxin E binding Domain Recombinant Protein in Mice. J. Mazandaran Univ. Med. Sci. 2015;25(124):37-47.
30. Buelow R, O'Hehir R, Schreifels R, Kummerehl T, Riley G, Lamb J. Localization of the immunologic activity in the superantigen Staphylococcal enterotoxin B using truncated recombinant fusion proteins. J. Immunol. 1992;148(1):1-6.
31. Shang L, Nienhaus K, Nienhaus GU. Engineered nanoparticles interacting with cells: size matters. J. Nanobiotechnol. 2014;12(1):5.
32. Stiles BG, Garza AR, Ulrich RG, Boles JW. Mucosal vaccination with recombinantly attenuated staphylococcal enterotoxin B and protection in a murine model. Infect. Immun. 2001;69(4):2031-6.
33. Bagheripour M, Ebrahimi F, Hajizadeh A, Nazarian S, Arefpour M. Preparation of chitosan-based botulinum neurotoxin e recombinant nanovaccine and evaluation of its immunogenicity as oral & intradermal route in mice. J RafsanjanUniv Med Sci 2016;14(11):923-38.
34. Fernández-Urrusuno R, Calvo P, Remuñán-López C, Vila-Jato JL, Alonso MJ. Enhancement of nasal absorption of insulin using chitosan nanoparticles. Pharm. Res. 1999;16(10):1576-81.
35. Amini Y, Tebianian M, Mosavari N, Fasihi Ramandi M, Ebrahimi S, Dabaghian M, et al. Preparation of ESAT-6 Nanoparticles and Evaluation of Humoral Immunity after Intranasal Administration. JSSU. 2013;20(5):612-26.
| Files | ||
| Issue | Vol 19, No 2 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v19i2.2767 | |
| PMID | 32372629 | |
| Keywords | ||
| Chitosan Intranasal administration Nanoparticles Staphylococcusaureus Staphylococcal enterotoxin B Vaccines | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Hosseini SA, Nazarian S, Ebrahimi F, Hajizade A. Immunogenicity Evaluation of Recombinant Staphylococcus aureus Enterotoxin B (rSEB) and rSEB-loaded Chitosan Nanoparticles Following Nasal Administration. Iran J Allergy Asthma Immunol. 2020;19(2):159-171.
