Immunization of BALB/c Mice against Shigella sonnei Using a Multiepitope Protein Vaccine through Intranasal and Subcutaneous Administration
-
Shabnam Akhgar
,
Shamsi Noorpisheh Ghadimi
,
Ibrahim Farhani
,
Abdolmajid Ghasemian
,
Shirin Mahmoodi
,
Mehdi mardkhoshnood
,
Ali Zarenezhad
Abstract
As the most common cause of bacillary dysentery or shigellosis, Shigella sonnei (S nonnei) has spread throughout the world. Invasion of the colorectal epithelial cells by this facultative intracellular bacterium occurs via various virulence factors. The increase in the resistance rate highlights the need for novel interventions, particularly increasing the urgency of the development of Shigella vaccines that may offer an effective solution.
A multiepitope protein vaccine (MEPV) construct previously designed using bioinformatics tools against Shigella species, was applied in vivo in BALB/C mice. The designed vaccine construct was expressed in a bacterial host, purified, and finally confirmed by Western blot analysis.
The immunogenicity of the purified MEPV was assessed against S sonnei via intranasal and subcutaneous administration routes, followed by evaluating its protective efficiency. We observed that interferon-gamma, interleukin-4, and immunoglobulin G levels were increased in all experimental groups.
Therefore, The MEPV effectively protected the mice against S sonnei.
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2. Baker S, The HC. Recent insights into Shigella: a major contributor to the global diarrhoeal disease burden. Curr Opin Infect Dis. 2018;31(5):449.
3. Song YJ, Cheong HK, Ki M, Shin JY, Hwang SS, Park M, et al. The Epidemiological Influence of Climatic Factors on Shigellosis Incidence Rates in Korea. Int J Environ Res Public Health. 2018;15(10).
4. Chao DL, Roose A, Roh M, Kotloff KL, Proctor JL. The seasonality of diarrheal pathogens: A retrospective study of seven sites over three years. PLoS Negl Trop Dis. 2019;13(8):e0007211.
5. Raso MM, Arato V, Gasperini G, Micoli F. Toward a Shigella Vaccine: Opportunities and Challenges to Fight an Antimicrobial-Resistant Pathogen. Int J Mol Sci. 2023;24(5):4649.
6. Moradi F, Hadi N, Akbari M, Hashemizadeh Z, Rouhi Jahromi R. Frequency and Antimicrobial Resistance of Shigella Species in Iran During 2000-2020. Jundishapur J Health Sci. 2021;13(2):e114902.
7. Camacho AI, Irache JM, Gamazo C. Recent progress towards development of a Shigella vaccine. Expert Rev Vaccines. 2013;12(1):43-55.
8. Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Org. 1999;77(8):651.
9. Kar AK, Ghosh AS, Chauhan K, Ahamed J, Basu J, Chakrabarti P, et al. Involvement of a 43-kilodalton outer membrane protein in beta-lactam resistance of Shigella dysenteriae. Antimicrob Agents Chemother. 1997;41(10):2302-4.
10. Raja SB, Murali MR, Devaraj SN. Differential expression of ompC and ompF in multidrug-resistant Shigella dysenteriae and Shigella flexneri by aqueous extract of Aegle marmelos, altering its susceptibility toward β-lactam antibiotics. Diagn Microbiol Infect Dis. 2008;61(3):321-8.
11. Bardsley M, Jenkins C, Mitchell HD, Mikhail AFW, Baker KS, Foster K, et al. Persistent Transmission of Shigellosis in England Is Associated with a Recently Emerged Multidrug-Resistant Strain of Shigella sonnei. J Clin Microbiol. 2020;58(4).
12. Moreno-Mingorance A, Mir-Cros A, Goterris L, Rodriguez-Garrido V, Sulleiro E, Barberà MJ, et al. Increasing trend of antimicrobial resistance in Shigella associated with MSM transmission in Barcelona, 2020-21: outbreak of XRD Shigella sonnei and dissemination of ESBL-producing Shigella flexneri. J Antimicrob Chemother. 2023;78(4):975-82.
13. Ranjbar R, Farahani A. Shigella: antibiotic-resistance mechanisms and new horizons for treatment. Infect Drug Resist. 2019;12:3137.
14. Rasolofo-Razanamparany V, Cassel-Beraud A-M, Roux J, Sansonetti PJ, Phalipon A. Predominance of serotype-specific mucosal antibody response in Shigella flexneri-infected humans living in an area of endemicity. Infect Immun. 2001;69(9):5230-4.
15. Herrera CM, Schmitt JS, Chowdhry EI, Riddle MS.
From Kiyoshi Shiga to Present-Day Shigella Vaccines: A
Historical Narrative Review. Vaccines. 2022;10(5):645.
16. Ranallo RT, Fonseka S, Boren TL, Bedford LA, Kaminski RW, Thakkar S, et al. Two live attenuated Shigella flexneri 2a strains WRSf2G12 and WRSf2G15: a new combination of gene deletions for 2nd generation live attenuated vaccine candidates. Vaccine. 2012;30(34):5159-71.
17. Shim D-H, Chang S-Y, Park S-M, Jang H, Carbis R, Czerkinsky C, et al. Immunogenicity and protective efficacy offered by a ribosomal-based vaccine from Shigella flexneri 2a. Vaccine. 2007;25(25):4828-36.
18. Riddle MS, Kaminski RW, Williams C, Porter C, Baqar S, Kordis A, et al. Safety and immunogenicity of an intranasal Shigella flexneri 2a Invaplex 50 vaccine. Vaccine. 2011;29(40):7009-19.
19. Karthik L, Kumar G, Keswani T, Bhattacharyya A, Chandar SS, Bhaskara Rao K. Protease inhibitors from marine actinobacteria as a potential source for antimalarial compound. PloS one. 2014;9(3):e90972.
20. Vakili B, Nezafat N, Zare B, Erfani N, Akbari M, Ghasemi Y, et al. A new multiepitope peptide vaccine induces immune responses and protection against Leishmania infantum in BALB/c mice. Med Microbiol Immunol. 2020;209(1):69-79.
21. Ashkenazi S, Cohen D. An update on vaccines against Shigella. Ther Adv Vaccines. 2013;1(3):113-23.
22. Anderson M, Sansonetti PJ, Marteyn BS. Shigella diversity and changing landscape: insights for the twenty-first century. Front Cell Infect Microbiol. 2016;6:45.
23. Martinez-Becerra FJ, Kissmann JM, Diaz-McNair J, Choudhari SP, Quick AM, Mellado-Sanchez G, et al. Broadly protective Shigella vaccine based on type III secretion apparatus proteins. Infect Immun. 2012;80(3):1222-31.
24. Farhani I, Nezafat N, Mahmoodi S. Designing a Novel Multiepitope Peptide Vaccine Against Pathogenic Shigella spp. Based Immunoinformatics Approaches. Int J Pept Res Ther. 2019;25(2):541-53.
25. Skountzou I, del Pilar Martin M, Wang B, Ye L, Koutsonanos D, Weldon W, et al. Salmonella flagellins are potent adjuvants for intranasally administered whole inactivated influenza vaccine. Vaccine. 2010;28(24):4103-12.
26. Wang C, Zhu W, Luo Y, Wang B-Z. Gold nanoparticles conjugating recombinant influenza hemagglutinin trimers and flagellin enhanced mucosal cellular immunity. Nanomedicine. 2018;14(4):1349-60.
27. Khalouie F, Mousavi SL, Nazarian S, Amani J, Pourfarzam P. Immunogenic evaluation of chimeric recombinant protein against ETEC, EHEC and Shigella. Mol Biol Res Commun. 2017;6(3):101.
28. Shilling PJ, Mirzadeh K, Cumming AJ, Widesheim M, Köck Z, Daley DO. Improved designs for pET expression plasmids increase protein production yield in Escherichia coli. Commun Biol. 2020;3(1):214.
29. Motamedi Dehbarez F, Mahmoodi S. Production of a Novel Multiepitope Peptide Vaccine against Hepatocellular Carcinoma. Iran J Med Sci. 2022;47(6):558-65.
30. Gu Y, Sun X, Li B, Huang J, Zhan B, Zhu X. Vaccination with a Paramyosin-Based Multiepitope Vaccine Elicits Significant Protective Immunity against Trichinella spiralis Infection in Mice. Front Microbiol. 2017;8.
31. León Y, Zapata L, Molina RE, Okanovič G, Gómez LA, Daza-Castro C, et al. Intranasal Immunization of Mice with Multiepitope Chimeric Vaccine Candidate Based on Conserved Autotransporters SigA, Pic and Sap, Confers Protection against Shigella flexneri. Vaccines (Basel). 2020;8(4).
32. Ramirez K, Capozzo AV, Lloyd SA, Sztein MB, Nataro JP, Pasetti MF. Mucosally delivered Salmonella typhi expressing the Yersinia pestis F1 antigen elicits mucosal and systemic immunity early in life and primes the neonatal immune system for a vigorous anamnestic response to parenteral F1 boost. J Immunol. 2009;182(2):1211-22.
33. Mallett C, VanDeVerg L, Collins H, Hale T. Evaluation of Shigella vaccine safety and efficacy in an intranasally challenged mouse model. Vaccine. 1993;11(2):190-6.
34. van de Verg LL, Mallett CP, Collins HH, Larsen T, Hammack C, Hale TL. Antibody and cytokine responses in a mouse pulmonary model of Shigella flexneri serotype 2a infection. Infect Immun. 1995;63(5):1947-54.
35. Kotloff KL, Riddle MS, Platts-Mills JA, Pavlinac P, Zaidi AK. Shigellosis. Lancet. 2018;391(10122):801-12.
36. Shad AA, Shad WA. Shigella sonnei: virulence and antibiotic resistance. Arch Microbiol. 2021;203(1):45-58.
37. Martinez-Becerra FJ, Chen X, Dickenson NE, Choudhari SP, Harrison K, Clements JD, et al. Characterization of a novel fusion protein from IpaB and IpaD of Shigella spp. and its potential as a pan-Shigella vaccine. Infect Immun. 2013;81(12):4470-7.
38. Talebreza A, Memariani M, Memariani H, Shirazi MH, Eghbali Shamsabad P, Bakhtiari M. Prevalence and Antibiotic Susceptibility of Shigella Species Isolated From Pediatric Patients in Tehran. Arch Pediatr Infect Dis. 2016;4(1):e32395.
39. Baseer S, Ahmad S, Ranaghan KE, Azam SS. Towards a peptide-based vaccine against Shigella sonnei: A subtractive reverse vaccinology based approach. Biologicals. 2017;50:87-99.
40. León Y, Zapata L, Molina RE, Okanovič G, Gómez LA, Daza-Castro C, et al. Intranasal immunization of mice with multiepitope chimeric vaccine candidate based on conserved autotransporters SigA, Pic and Sap, confers protection against Shigella flexneri. Vaccines. 2020;8(4):563.
41. Barzu S, Nato F, Rouyre S, Mazie J-C, Sansonetti P, Phalipon A. Characterization of B-cell epitopes on IpaB, an invasion-associated antigen of Shigella flexneri: identification of an immunodominant domain recognized during natural infection. Infect Immun. 1993;61(9):3825-31.
42. Purcell AW, McCluskey J, Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov. 2007;6(5):404-14.
43. Jo SH, Lee J, Park E, Kim DW, Lee DH, Ryu CM, et al. A human pathogenic bacterium Shigella proliferates in plants through adoption of type III effectors for shigellosis. Plant Cell Environ. 2019;42(11):2962-78.
44. Raqib R, Lindberg AA, Wretlind B, Bardhan PK, Andersson U, Andersson J. Persistence of local cytokine production in shigellosis in acute and convalescent stages. Infect Immun. 1995;63(1):289-96.
45. Nosrati M, Hajizade A, Nazarian S, Amani J, Namvar Vansofla A, Tarverdizadeh Y. Designing a multiepitope vaccine for cross-protection against Shigella spp: An immunoinformatics and structural vaccinology study. Mol Immunol. 2019;116:106-16.
46. Namvar A, Hajizade A, Nazarian S, Sadeghi D, Akbari MR, Tarverdizade Y. Design and Recombinant Expression of a multiepitope Vaccine Candidate Against Pathogenic Species of Shigella. Vaccine Res. 2021;8(1):18-22.
47. Chitradevi STS, Kaur G, Uppalapati S, Yadav A, Singh D, Bansal A. Co-administration of rIpaB domain of Shigella with rGroEL of S. Typhi enhances the immune responses and protective efficacy against Shigella infection. Cell Mol Immunol. 2015;12(6):757-67.
48. Pore D, Mahata N, Pal A, Chakrabarti MK. Outer membrane protein A (OmpA) of Shigella flexneri 2a, induces protective immune response in a mouse model. PloS one. 2011;6(7):e22663.
49. Gilavand F, Marzban A, Ebrahimipour G, Soleimani N, Goudarzi M. Designation of chitosan nano-vaccine based on MxiH antigen of Shigella flexneri with increased immunization capacity. Carbohydr Polym. 2020;232:115813.
50. Bansal A, Paliwal PK, Sagi SS, Sairam M. Effect of adjuvants on immune response and protective immunity elicited by recombinant Hsp60 (GroEL) of Salmonella typhi against S. typhi infection. Mol Cell Biochem. 2010;337(1):213-21.
51. Behmard E, Abdulabbas HT, Abdalkareem Jasim S, Najafipour S, Ghasemian A, Farjadfar A, et al. Design of a novel multiepitope vaccine candidate against hepatitis C virus using structural and nonstructural proteins: An immunoinformatics approach. PLoS One. 2022;17(8):e0272582.
52. Zhang Y, Zhao G, Xiong Y, Li F, Chen Y, Cheng Y, et al. Development of a Universal Multiepitope Vaccine Candidate against Streptococcus suis Infections Using Immunoinformatics Approaches. Vet Sci . 2023;10(6):383.
2. Baker S, The HC. Recent insights into Shigella: a major contributor to the global diarrhoeal disease burden. Curr Opin Infect Dis. 2018;31(5):449.
3. Song YJ, Cheong HK, Ki M, Shin JY, Hwang SS, Park M, et al. The Epidemiological Influence of Climatic Factors on Shigellosis Incidence Rates in Korea. Int J Environ Res Public Health. 2018;15(10).
4. Chao DL, Roose A, Roh M, Kotloff KL, Proctor JL. The seasonality of diarrheal pathogens: A retrospective study of seven sites over three years. PLoS Negl Trop Dis. 2019;13(8):e0007211.
5. Raso MM, Arato V, Gasperini G, Micoli F. Toward a Shigella Vaccine: Opportunities and Challenges to Fight an Antimicrobial-Resistant Pathogen. Int J Mol Sci. 2023;24(5):4649.
6. Moradi F, Hadi N, Akbari M, Hashemizadeh Z, Rouhi Jahromi R. Frequency and Antimicrobial Resistance of Shigella Species in Iran During 2000-2020. Jundishapur J Health Sci. 2021;13(2):e114902.
7. Camacho AI, Irache JM, Gamazo C. Recent progress towards development of a Shigella vaccine. Expert Rev Vaccines. 2013;12(1):43-55.
8. Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Org. 1999;77(8):651.
9. Kar AK, Ghosh AS, Chauhan K, Ahamed J, Basu J, Chakrabarti P, et al. Involvement of a 43-kilodalton outer membrane protein in beta-lactam resistance of Shigella dysenteriae. Antimicrob Agents Chemother. 1997;41(10):2302-4.
10. Raja SB, Murali MR, Devaraj SN. Differential expression of ompC and ompF in multidrug-resistant Shigella dysenteriae and Shigella flexneri by aqueous extract of Aegle marmelos, altering its susceptibility toward β-lactam antibiotics. Diagn Microbiol Infect Dis. 2008;61(3):321-8.
11. Bardsley M, Jenkins C, Mitchell HD, Mikhail AFW, Baker KS, Foster K, et al. Persistent Transmission of Shigellosis in England Is Associated with a Recently Emerged Multidrug-Resistant Strain of Shigella sonnei. J Clin Microbiol. 2020;58(4).
12. Moreno-Mingorance A, Mir-Cros A, Goterris L, Rodriguez-Garrido V, Sulleiro E, Barberà MJ, et al. Increasing trend of antimicrobial resistance in Shigella associated with MSM transmission in Barcelona, 2020-21: outbreak of XRD Shigella sonnei and dissemination of ESBL-producing Shigella flexneri. J Antimicrob Chemother. 2023;78(4):975-82.
13. Ranjbar R, Farahani A. Shigella: antibiotic-resistance mechanisms and new horizons for treatment. Infect Drug Resist. 2019;12:3137.
14. Rasolofo-Razanamparany V, Cassel-Beraud A-M, Roux J, Sansonetti PJ, Phalipon A. Predominance of serotype-specific mucosal antibody response in Shigella flexneri-infected humans living in an area of endemicity. Infect Immun. 2001;69(9):5230-4.
15. Herrera CM, Schmitt JS, Chowdhry EI, Riddle MS.
From Kiyoshi Shiga to Present-Day Shigella Vaccines: A
Historical Narrative Review. Vaccines. 2022;10(5):645.
16. Ranallo RT, Fonseka S, Boren TL, Bedford LA, Kaminski RW, Thakkar S, et al. Two live attenuated Shigella flexneri 2a strains WRSf2G12 and WRSf2G15: a new combination of gene deletions for 2nd generation live attenuated vaccine candidates. Vaccine. 2012;30(34):5159-71.
17. Shim D-H, Chang S-Y, Park S-M, Jang H, Carbis R, Czerkinsky C, et al. Immunogenicity and protective efficacy offered by a ribosomal-based vaccine from Shigella flexneri 2a. Vaccine. 2007;25(25):4828-36.
18. Riddle MS, Kaminski RW, Williams C, Porter C, Baqar S, Kordis A, et al. Safety and immunogenicity of an intranasal Shigella flexneri 2a Invaplex 50 vaccine. Vaccine. 2011;29(40):7009-19.
19. Karthik L, Kumar G, Keswani T, Bhattacharyya A, Chandar SS, Bhaskara Rao K. Protease inhibitors from marine actinobacteria as a potential source for antimalarial compound. PloS one. 2014;9(3):e90972.
20. Vakili B, Nezafat N, Zare B, Erfani N, Akbari M, Ghasemi Y, et al. A new multiepitope peptide vaccine induces immune responses and protection against Leishmania infantum in BALB/c mice. Med Microbiol Immunol. 2020;209(1):69-79.
21. Ashkenazi S, Cohen D. An update on vaccines against Shigella. Ther Adv Vaccines. 2013;1(3):113-23.
22. Anderson M, Sansonetti PJ, Marteyn BS. Shigella diversity and changing landscape: insights for the twenty-first century. Front Cell Infect Microbiol. 2016;6:45.
23. Martinez-Becerra FJ, Kissmann JM, Diaz-McNair J, Choudhari SP, Quick AM, Mellado-Sanchez G, et al. Broadly protective Shigella vaccine based on type III secretion apparatus proteins. Infect Immun. 2012;80(3):1222-31.
24. Farhani I, Nezafat N, Mahmoodi S. Designing a Novel Multiepitope Peptide Vaccine Against Pathogenic Shigella spp. Based Immunoinformatics Approaches. Int J Pept Res Ther. 2019;25(2):541-53.
25. Skountzou I, del Pilar Martin M, Wang B, Ye L, Koutsonanos D, Weldon W, et al. Salmonella flagellins are potent adjuvants for intranasally administered whole inactivated influenza vaccine. Vaccine. 2010;28(24):4103-12.
26. Wang C, Zhu W, Luo Y, Wang B-Z. Gold nanoparticles conjugating recombinant influenza hemagglutinin trimers and flagellin enhanced mucosal cellular immunity. Nanomedicine. 2018;14(4):1349-60.
27. Khalouie F, Mousavi SL, Nazarian S, Amani J, Pourfarzam P. Immunogenic evaluation of chimeric recombinant protein against ETEC, EHEC and Shigella. Mol Biol Res Commun. 2017;6(3):101.
28. Shilling PJ, Mirzadeh K, Cumming AJ, Widesheim M, Köck Z, Daley DO. Improved designs for pET expression plasmids increase protein production yield in Escherichia coli. Commun Biol. 2020;3(1):214.
29. Motamedi Dehbarez F, Mahmoodi S. Production of a Novel Multiepitope Peptide Vaccine against Hepatocellular Carcinoma. Iran J Med Sci. 2022;47(6):558-65.
30. Gu Y, Sun X, Li B, Huang J, Zhan B, Zhu X. Vaccination with a Paramyosin-Based Multiepitope Vaccine Elicits Significant Protective Immunity against Trichinella spiralis Infection in Mice. Front Microbiol. 2017;8.
31. León Y, Zapata L, Molina RE, Okanovič G, Gómez LA, Daza-Castro C, et al. Intranasal Immunization of Mice with Multiepitope Chimeric Vaccine Candidate Based on Conserved Autotransporters SigA, Pic and Sap, Confers Protection against Shigella flexneri. Vaccines (Basel). 2020;8(4).
32. Ramirez K, Capozzo AV, Lloyd SA, Sztein MB, Nataro JP, Pasetti MF. Mucosally delivered Salmonella typhi expressing the Yersinia pestis F1 antigen elicits mucosal and systemic immunity early in life and primes the neonatal immune system for a vigorous anamnestic response to parenteral F1 boost. J Immunol. 2009;182(2):1211-22.
33. Mallett C, VanDeVerg L, Collins H, Hale T. Evaluation of Shigella vaccine safety and efficacy in an intranasally challenged mouse model. Vaccine. 1993;11(2):190-6.
34. van de Verg LL, Mallett CP, Collins HH, Larsen T, Hammack C, Hale TL. Antibody and cytokine responses in a mouse pulmonary model of Shigella flexneri serotype 2a infection. Infect Immun. 1995;63(5):1947-54.
35. Kotloff KL, Riddle MS, Platts-Mills JA, Pavlinac P, Zaidi AK. Shigellosis. Lancet. 2018;391(10122):801-12.
36. Shad AA, Shad WA. Shigella sonnei: virulence and antibiotic resistance. Arch Microbiol. 2021;203(1):45-58.
37. Martinez-Becerra FJ, Chen X, Dickenson NE, Choudhari SP, Harrison K, Clements JD, et al. Characterization of a novel fusion protein from IpaB and IpaD of Shigella spp. and its potential as a pan-Shigella vaccine. Infect Immun. 2013;81(12):4470-7.
38. Talebreza A, Memariani M, Memariani H, Shirazi MH, Eghbali Shamsabad P, Bakhtiari M. Prevalence and Antibiotic Susceptibility of Shigella Species Isolated From Pediatric Patients in Tehran. Arch Pediatr Infect Dis. 2016;4(1):e32395.
39. Baseer S, Ahmad S, Ranaghan KE, Azam SS. Towards a peptide-based vaccine against Shigella sonnei: A subtractive reverse vaccinology based approach. Biologicals. 2017;50:87-99.
40. León Y, Zapata L, Molina RE, Okanovič G, Gómez LA, Daza-Castro C, et al. Intranasal immunization of mice with multiepitope chimeric vaccine candidate based on conserved autotransporters SigA, Pic and Sap, confers protection against Shigella flexneri. Vaccines. 2020;8(4):563.
41. Barzu S, Nato F, Rouyre S, Mazie J-C, Sansonetti P, Phalipon A. Characterization of B-cell epitopes on IpaB, an invasion-associated antigen of Shigella flexneri: identification of an immunodominant domain recognized during natural infection. Infect Immun. 1993;61(9):3825-31.
42. Purcell AW, McCluskey J, Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov. 2007;6(5):404-14.
43. Jo SH, Lee J, Park E, Kim DW, Lee DH, Ryu CM, et al. A human pathogenic bacterium Shigella proliferates in plants through adoption of type III effectors for shigellosis. Plant Cell Environ. 2019;42(11):2962-78.
44. Raqib R, Lindberg AA, Wretlind B, Bardhan PK, Andersson U, Andersson J. Persistence of local cytokine production in shigellosis in acute and convalescent stages. Infect Immun. 1995;63(1):289-96.
45. Nosrati M, Hajizade A, Nazarian S, Amani J, Namvar Vansofla A, Tarverdizadeh Y. Designing a multiepitope vaccine for cross-protection against Shigella spp: An immunoinformatics and structural vaccinology study. Mol Immunol. 2019;116:106-16.
46. Namvar A, Hajizade A, Nazarian S, Sadeghi D, Akbari MR, Tarverdizade Y. Design and Recombinant Expression of a multiepitope Vaccine Candidate Against Pathogenic Species of Shigella. Vaccine Res. 2021;8(1):18-22.
47. Chitradevi STS, Kaur G, Uppalapati S, Yadav A, Singh D, Bansal A. Co-administration of rIpaB domain of Shigella with rGroEL of S. Typhi enhances the immune responses and protective efficacy against Shigella infection. Cell Mol Immunol. 2015;12(6):757-67.
48. Pore D, Mahata N, Pal A, Chakrabarti MK. Outer membrane protein A (OmpA) of Shigella flexneri 2a, induces protective immune response in a mouse model. PloS one. 2011;6(7):e22663.
49. Gilavand F, Marzban A, Ebrahimipour G, Soleimani N, Goudarzi M. Designation of chitosan nano-vaccine based on MxiH antigen of Shigella flexneri with increased immunization capacity. Carbohydr Polym. 2020;232:115813.
50. Bansal A, Paliwal PK, Sagi SS, Sairam M. Effect of adjuvants on immune response and protective immunity elicited by recombinant Hsp60 (GroEL) of Salmonella typhi against S. typhi infection. Mol Cell Biochem. 2010;337(1):213-21.
51. Behmard E, Abdulabbas HT, Abdalkareem Jasim S, Najafipour S, Ghasemian A, Farjadfar A, et al. Design of a novel multiepitope vaccine candidate against hepatitis C virus using structural and nonstructural proteins: An immunoinformatics approach. PLoS One. 2022;17(8):e0272582.
52. Zhang Y, Zhao G, Xiong Y, Li F, Chen Y, Cheng Y, et al. Development of a Universal Multiepitope Vaccine Candidate against Streptococcus suis Infections Using Immunoinformatics Approaches. Vet Sci . 2023;10(6):383.
| Files | ||
| Issue | Vol 23 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v23i4.16215 | |
| Keywords | ||
| Adjuvant Immunogenicity Shigella sonnei Vaccines | ||
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How to Cite
1.
Akhgar S, Noorpisheh Ghadimi S, Farhani I, Ghasemian A, Mahmoodi S, mardkhoshnood M, Zarenezhad A. Immunization of BALB/c Mice against Shigella sonnei Using a Multiepitope Protein Vaccine through Intranasal and Subcutaneous Administration. Iran J Allergy Asthma Immunol. 2024;23(4):412-421.
