Immuno-proteomics analysis between OMV of vaccine and dominant wild type strains of Bordetella pertussis in Iran
-
Ali Badamchi
,
Fariborz Bahrami
,
Alireza Hadizadeh Tasbiti
,
Shamsi Yari
,
Morvarid Shafiei
,
Fereshteh Shahcheraghi
,
Seyed Davar Siadat
Abstract
Background and Objectives: Despite widespread vaccination programs against pertussis, there has been a worldwide resurgence of the disease in recent years. We aimed to investigate protein composition of outer membrane vesicles (OMV) of Bordetella pertussis (Bp) and to evaluate the immunogenicity of OMV antigens both in the vaccine and the dominant wild type strains in Iran.
Materials and Methods: The OMV were purified from both vaccine and wild type strains. The immunoreactivity of the OMVs was investigated by exposing sera taken from the patients and the vaccinated infants. The protein profiles of OMVs were compared using two-dimensional electrophoresis. The LC-MS/MS was used to analyse and identify differentially expressed protein spots.
Results: The two type strains showed differences in their 2D gel protein profile. Further analysis of selected proteins from the dominant Iranian strains using LC-MS/MS demonstrated that the identified proteins fell into different functional categories including (i) metabolism, (ii) membrane transport and secretion system, (iii) biosynthesis and degradation, (iv) adaption, adhesion, pathogenicity, conserved hypothetical and protection responses. Moreover, a number of immunogenic proteins were identified including Bp 2434 (serine protease) and Bp 1616 (putative DNA binding protein) from the vaccine and the wild type strains, respectively which could be considered as potential antigens for an OMV vaccine.
Conclusion: OMV Bp could be considered as an alternative vaccine against pertussis, containing the bacterium’s protein antigens that can confer equal efficacy compared to a whole bacterial cell vaccine with advantages such as less side effects and lower costs than acellular pertussis vaccines.
1. Folaranmi T, Pinell-McNamara V, Griffith M, Hao Y, Coronado F, Briere EC. Systematic review and meta-analysis of pertussis epidemiology in Latin America and the Caribbean: 1980–2015. Rev Panam Salud Publica 2017; 41: e102.
2. World Health Organization. Pertussis vaccines: Who position paper. Wkly Epidemiol Rec 2015; 90: 433-460.
3. Klein NP. Licensed pertussis vaccines in the United States: history and current state. Hum Vaccin Immunother 2014;10:2684-2690.
4. Ryan EJ, Nilsson L, Kjellman NI, Gothefors L, Mills KH. Booster immunization of children with an acellular pertussis vaccine enhances Th2 cytokine production and serum IgE responses against pertussis toxin but not against common allergens. Clin Exp Immunol 2000; 121:193-200.
5. Gambhir M, Clark TA, Cauchemez S, Tartof SY, Swerdlow DL, Ferguson NM. A change in vaccine efficacy and duration of protection explains recent rises in pertussis incidence in the United States. PLoS Comput Biol 2015; 11(4):e1004138.
6. Cherry JD. Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med 2012; 367:785-787.
7. Park SB, Jang HB, Nho SW, Cha IS, Hikima JI, Ohtani M, et al. Outer membrane vesicles as a candidate vaccine against edwardsiellosis. PLoS One 2011; 6(3):e17629.
8. Raeven RH, van der Maas L, Tilstra W, Uittenbogaard JP, Bindels TH, Kuipers B, et al. Immunoproteomic profiling of Bordetella pertussis outer membrane vesicle vaccine reveals broad and balanced humoral immunogenicity. J Proteome Res 2015; 14:2929-2942.
9. Hozbor D, Rodriguez ME, Fernandez J, Lagares A, Guiso N, Yantorno O. Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 1999; 38:273-278.
10. Heravi FS, Nikbin VS, Lotfi MN, Badiri P, Ahmadi NJ, Zahraei SM, et al. Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis 2018;37:1893-1900.
11. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.
12. Hendrikx LH, Öztürk K, De Rond LG, De Greeff SC, Sanders EA, Berbers GA, et al. Serum IgA responses against pertussis proteins in infected and Dutch wP or aP vaccinated children: an additional role in pertussis diagnostics. PLoS One 2011; 6(11):e27681.
13. Yari S, Tasbiti AH, Ghanei M, Shokrgozar MA, Vaziri B, Mahdian R, et al. Proteomic analysis of sensitive and multi drug resistant Mycobacterium tuberculosis strains. Microbiology 2016; 85:350-358.
14. Pérez A, Merino M, Rumbo-Feal S, Álvarez-Fraga L, Vallejo JA, Beceiro A, et al . The FhaB/FhaC two-partner secretion system is involved in adhesion of Acinetobacter baumannii AbH12O-A2 strain. Virulence 2017; 8:959-974.
15. Saha S, Raghava GP. Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins 2006; 65:40-48.
16. Gardy JL, Laird MR, Chen F, Rey S, Walsh CJ, Ester M, et al. PSORTb v.2. 0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005; 21: 617-623.
17. Asensio CJ, Gaillard ME, Moreno G, Bottero D, Zurita E, Rumbo M, et al. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 2011; 29:1649-1656.
18. Kim YH, Kim KA, Kim YR, Choi MK, Kim HK, Choi KJ, et al. Immunoproteomically identified GBAA _0345, alkyl hydroperoxide reductase subunit C is a potential target for multivalent anthrax vaccine. Proteomics 2014;14:93-104.
19. Chen Z, He Q. Immune persistence after pertussis vaccination. Hum Vaccin Immunother 2017; 13:744-756.
20. Robbins JB, Schneerson R, Kubler-Kielb J, Keith JM, Trollfors B, Vinogradov E, et al. Toward a new vaccine for pertussis. Proc Natl Acad Sci U S A 2014; 111:3213-3216.
21. Asl YM, Akhi MT, Soroush MH, Sefidan FY, Mousapour J, Hejazi ME, et al. Clinical Manifestations and Seasonality of Pertussis in Azerbaijan, Iran. Infect Dis Clin Pract 2018; 26:145-149.
22. Greco D, Salmaso S, Mastrantonio P, Giuliano M, Tozzi AE, Anemona A, et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. N Engl J Med 1996; 334:341-348.
23. Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N Engl J Med 1996; 334:349-355.
24. Blennow M, Hedenskog S, Granström M. Protective effect of acellular pertussis vaccines. Eur J Clin Microbiol Infect Dis 1988; 7:381-383.
25. De Greeff SC, De Melker HE, Van Gageldonk PG, Schellekens JF, van der Klis FR, Mollema L, et al. Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis. PLoS One 2010; 5(12): e14183.
26. van der Maas NA, Mooi FR, de Greeff SC, Berbers GA, Conyn-van Spaendonck MA, de Melker HE. Pertussis in the Netherlands, is the current vaccination strategy sufficient to reduce disease burden in young infants. Vaccine 2013; 31:4541-4547.
27. Zhao Z, Xue Y, Tang X, Wu B, Cheng X, He Q, et al . Immunogenicity of recombinant protective antigen and efficacy against intranasal challenge with Bordetella bronchiseptica. Vaccine 2009; 27:2523-2528.
28. Sobota JM, Imlay JA. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci U S A 2011; 108:5402-5407.
29. Gu M , Imlay JA. Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol Microbiol 2013; 89:123-134.
30. Reynolds C, Goudet A, Jenjaroen K, Sumonwiriya M, Rinchai D, Musson J, et al. T Cell Immunity to the Alkyl Hydroperoxide Reductase of Burkholderia pseudomallei: a correlate of disease outcome in acute melioidosis. J Immunol 2015; 194:4814-4824.
31. Shinoy M, Dennehy R, Coleman L, Carberry S, Schaffer K, Callaghan M, et al. Immunoproteomic analysis of proteins expressed by two related pathogens, Burkholderia multivorans and Burkholderia cenocepacia, during human infection. PLoS One 2013;8(11): e80796.
32. Velineni S, Timoney JF. Identification of novel immunoreactive proteins of Streptococcus zooepidemicus with potential as vaccine components. Vaccine 2013; 31:4129-4135.
33. O’Riordan AA, Morales VA, Mulligan L, Faheem N, Windle HJ, Kelleher DP. Alkyl hydroperoxide reductase: a candidate Helicobacter pylori vaccine. Vaccine 2012; 30:3876-3884.
34. Zhao Z, Xue Y, Tang X, Wu B, Cheng X, He Q. Immunogenicity of recombinant protective antigen and efficacy against intranasal challenge with Bordetella bronchiseptica. Vaccine 2009; 27:2523-2528.
35. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 2006;188:5385-5392.
36. Liu Y, Chen H, Wei Q, Xiao C, Ji Q, Bao G. Immune efficacy of five novel recombinant Bordetella bronchiseptica proteins. BMC Vet Res 2015; 11:173.
37. Tefon BE, Maaß S, Özcengiz E, Becher D, Hecker M, Özcengiz G. A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins. Vaccine 2011; 29:3583-3595.
38. Ruiz-Perez F, Wahid R, Faherty CS, Kolappaswamy K, Rodriguez L, Santiago A, et al. Serine protease autotransporters from Shigella flexneri and pathogenic Escherichia coli target a broad range of leukocyte glycoproteins. Proc Natl Acad Sci U S A 2011; 108:12881-12886.
39. Vijayakumar V, Santiago A, Smith R, Smith M, Robins-Browne RM, Nataro JP, et al. Role of a class 1 serine protease autotransporter in the pathogenesis of Citrobacter rodentium colitis. Infect Immun 2014: 82:2626-2636.
40. Altındiş E, Tefon BE, Yıldırım V, Özcengiz E, Becher D, Hecker M, et al. Immunoproteomic analysis of Bordetella pertussis and identification of new immunogenic proteins. Vaccine 2009; 27:542-548.
41. Yuk MH, Harvill ET, Cotter PA, Miller JF. Modulation of host immune responses, induction of apoptosis and inhibition of NF-κB activation by the Bordetella type III secretion system. Mol Microbiol 2000; 35:991-1004.
2. World Health Organization. Pertussis vaccines: Who position paper. Wkly Epidemiol Rec 2015; 90: 433-460.
3. Klein NP. Licensed pertussis vaccines in the United States: history and current state. Hum Vaccin Immunother 2014;10:2684-2690.
4. Ryan EJ, Nilsson L, Kjellman NI, Gothefors L, Mills KH. Booster immunization of children with an acellular pertussis vaccine enhances Th2 cytokine production and serum IgE responses against pertussis toxin but not against common allergens. Clin Exp Immunol 2000; 121:193-200.
5. Gambhir M, Clark TA, Cauchemez S, Tartof SY, Swerdlow DL, Ferguson NM. A change in vaccine efficacy and duration of protection explains recent rises in pertussis incidence in the United States. PLoS Comput Biol 2015; 11(4):e1004138.
6. Cherry JD. Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med 2012; 367:785-787.
7. Park SB, Jang HB, Nho SW, Cha IS, Hikima JI, Ohtani M, et al. Outer membrane vesicles as a candidate vaccine against edwardsiellosis. PLoS One 2011; 6(3):e17629.
8. Raeven RH, van der Maas L, Tilstra W, Uittenbogaard JP, Bindels TH, Kuipers B, et al. Immunoproteomic profiling of Bordetella pertussis outer membrane vesicle vaccine reveals broad and balanced humoral immunogenicity. J Proteome Res 2015; 14:2929-2942.
9. Hozbor D, Rodriguez ME, Fernandez J, Lagares A, Guiso N, Yantorno O. Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 1999; 38:273-278.
10. Heravi FS, Nikbin VS, Lotfi MN, Badiri P, Ahmadi NJ, Zahraei SM, et al. Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis 2018;37:1893-1900.
11. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.
12. Hendrikx LH, Öztürk K, De Rond LG, De Greeff SC, Sanders EA, Berbers GA, et al. Serum IgA responses against pertussis proteins in infected and Dutch wP or aP vaccinated children: an additional role in pertussis diagnostics. PLoS One 2011; 6(11):e27681.
13. Yari S, Tasbiti AH, Ghanei M, Shokrgozar MA, Vaziri B, Mahdian R, et al. Proteomic analysis of sensitive and multi drug resistant Mycobacterium tuberculosis strains. Microbiology 2016; 85:350-358.
14. Pérez A, Merino M, Rumbo-Feal S, Álvarez-Fraga L, Vallejo JA, Beceiro A, et al . The FhaB/FhaC two-partner secretion system is involved in adhesion of Acinetobacter baumannii AbH12O-A2 strain. Virulence 2017; 8:959-974.
15. Saha S, Raghava GP. Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins 2006; 65:40-48.
16. Gardy JL, Laird MR, Chen F, Rey S, Walsh CJ, Ester M, et al. PSORTb v.2. 0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005; 21: 617-623.
17. Asensio CJ, Gaillard ME, Moreno G, Bottero D, Zurita E, Rumbo M, et al. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 2011; 29:1649-1656.
18. Kim YH, Kim KA, Kim YR, Choi MK, Kim HK, Choi KJ, et al. Immunoproteomically identified GBAA _0345, alkyl hydroperoxide reductase subunit C is a potential target for multivalent anthrax vaccine. Proteomics 2014;14:93-104.
19. Chen Z, He Q. Immune persistence after pertussis vaccination. Hum Vaccin Immunother 2017; 13:744-756.
20. Robbins JB, Schneerson R, Kubler-Kielb J, Keith JM, Trollfors B, Vinogradov E, et al. Toward a new vaccine for pertussis. Proc Natl Acad Sci U S A 2014; 111:3213-3216.
21. Asl YM, Akhi MT, Soroush MH, Sefidan FY, Mousapour J, Hejazi ME, et al. Clinical Manifestations and Seasonality of Pertussis in Azerbaijan, Iran. Infect Dis Clin Pract 2018; 26:145-149.
22. Greco D, Salmaso S, Mastrantonio P, Giuliano M, Tozzi AE, Anemona A, et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. N Engl J Med 1996; 334:341-348.
23. Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N Engl J Med 1996; 334:349-355.
24. Blennow M, Hedenskog S, Granström M. Protective effect of acellular pertussis vaccines. Eur J Clin Microbiol Infect Dis 1988; 7:381-383.
25. De Greeff SC, De Melker HE, Van Gageldonk PG, Schellekens JF, van der Klis FR, Mollema L, et al. Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis. PLoS One 2010; 5(12): e14183.
26. van der Maas NA, Mooi FR, de Greeff SC, Berbers GA, Conyn-van Spaendonck MA, de Melker HE. Pertussis in the Netherlands, is the current vaccination strategy sufficient to reduce disease burden in young infants. Vaccine 2013; 31:4541-4547.
27. Zhao Z, Xue Y, Tang X, Wu B, Cheng X, He Q, et al . Immunogenicity of recombinant protective antigen and efficacy against intranasal challenge with Bordetella bronchiseptica. Vaccine 2009; 27:2523-2528.
28. Sobota JM, Imlay JA. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci U S A 2011; 108:5402-5407.
29. Gu M , Imlay JA. Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol Microbiol 2013; 89:123-134.
30. Reynolds C, Goudet A, Jenjaroen K, Sumonwiriya M, Rinchai D, Musson J, et al. T Cell Immunity to the Alkyl Hydroperoxide Reductase of Burkholderia pseudomallei: a correlate of disease outcome in acute melioidosis. J Immunol 2015; 194:4814-4824.
31. Shinoy M, Dennehy R, Coleman L, Carberry S, Schaffer K, Callaghan M, et al. Immunoproteomic analysis of proteins expressed by two related pathogens, Burkholderia multivorans and Burkholderia cenocepacia, during human infection. PLoS One 2013;8(11): e80796.
32. Velineni S, Timoney JF. Identification of novel immunoreactive proteins of Streptococcus zooepidemicus with potential as vaccine components. Vaccine 2013; 31:4129-4135.
33. O’Riordan AA, Morales VA, Mulligan L, Faheem N, Windle HJ, Kelleher DP. Alkyl hydroperoxide reductase: a candidate Helicobacter pylori vaccine. Vaccine 2012; 30:3876-3884.
34. Zhao Z, Xue Y, Tang X, Wu B, Cheng X, He Q. Immunogenicity of recombinant protective antigen and efficacy against intranasal challenge with Bordetella bronchiseptica. Vaccine 2009; 27:2523-2528.
35. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 2006;188:5385-5392.
36. Liu Y, Chen H, Wei Q, Xiao C, Ji Q, Bao G. Immune efficacy of five novel recombinant Bordetella bronchiseptica proteins. BMC Vet Res 2015; 11:173.
37. Tefon BE, Maaß S, Özcengiz E, Becher D, Hecker M, Özcengiz G. A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins. Vaccine 2011; 29:3583-3595.
38. Ruiz-Perez F, Wahid R, Faherty CS, Kolappaswamy K, Rodriguez L, Santiago A, et al. Serine protease autotransporters from Shigella flexneri and pathogenic Escherichia coli target a broad range of leukocyte glycoproteins. Proc Natl Acad Sci U S A 2011; 108:12881-12886.
39. Vijayakumar V, Santiago A, Smith R, Smith M, Robins-Browne RM, Nataro JP, et al. Role of a class 1 serine protease autotransporter in the pathogenesis of Citrobacter rodentium colitis. Infect Immun 2014: 82:2626-2636.
40. Altındiş E, Tefon BE, Yıldırım V, Özcengiz E, Becher D, Hecker M, et al. Immunoproteomic analysis of Bordetella pertussis and identification of new immunogenic proteins. Vaccine 2009; 27:542-548.
41. Yuk MH, Harvill ET, Cotter PA, Miller JF. Modulation of host immune responses, induction of apoptosis and inhibition of NF-κB activation by the Bordetella type III secretion system. Mol Microbiol 2000; 35:991-1004.
| Files | ||
| Issue | Vol 12 No 2 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i2.2610 | |
| Keywords | ||
| Bordetella pertussis; Outer membrane vesicles; Vaccine; Mass spectrometry analysis | ||
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How to Cite
1.
Badamchi A, Bahrami F, Hadizadeh Tasbiti A, Yari S, Shafiei M, Shahcheraghi F, Siadat SD. Immuno-proteomics analysis between OMV of vaccine and dominant wild type strains of Bordetella pertussis in Iran. Iran J Microbiol. 2020;12(2):77-88.
